Bettina Diekamp

Asymmetry pays: visual lateralization improves discrimination success in pigeons

Functional cerebral asymmetries, once thought to be exclusively human, are now accepted to be a widespread principle of brain organization in vertebrates [1]. The prevalence of lateralization makes it likely that it has some major advantage. Until now, however, conclusive evidence has been lacking. To analyze the relation between the extent of cerebral asymmetry and the degree of performance in visual foraging, we studied grain-grit discrimination success in pigeons, a species with a left hemisphere dominance for visual object processing [2,3]. The birds performed the task under left-eye, right-eye or binocular seeing conditions. In most animals, right-eye seeing was superior to left-eye seeing performance, and binocular performance was higher than each monocular level. The absolute difference between left- and right-eye levels was defined as a measure for the degree of visual asymmetry. Animals with higher asymmetries were more successful in discriminating grain from grit under binocular conditions. This shows that an increase in visual asymmetry enhances success in visually guided foraging. Possibly, asymmetries of the pigeons visual system increase the computational speed of object recognition processes by concentrating them into one hemisphere while preventing the other side of the brain from initiating conflicting search sequences of its own.

A left-sided visuospatial bias in birds

Document S1. Supplemental Experimental Procedures.xDownload (.03 MB ) Document S1. Supplemental Experimental Procedures.

Embryonic light stimulation induces different asymmetries in visuoperceptual and visuomotor pathways of pigeons

In birds, visual object discrimination performance is lateralized with a dominance of the right eye/left hemisphere. This asymmetry is induced by embryonic light stimulation. However, visually guided behavior, even during simple object distinction tasks, is composed of different behavioral and neural modules. Therefore, the aim of the present study was to test whether all neural subsystems involved in visual discriminations are lateralized in a similar way after prehatch visual stimulation. To examine this question, two behavioral paradigms were used which reveal complementary aspects of visually guided behavior. The first was the grain-grit discrimination task in which no left-right differences in the number of pecks, but significant differences in the number of grains can be found. Therefore, grain-grit discrimination reveals visuoperceptual performance but not visuomotor speed. The contrary seems to be the case for a successive pattern discrimination with a VR32 schedule. Here, the hemispheres do not differ with respect to discrimination accuracy but with regard to the number of pecks emitted. Thus, successive pattern discrimination with lean VR schedules reveals hemispheric differences in visuomotor speed without testing visuoperceptual performance. Using these two paradigms a group of light and a group of dark incubated pigeons were tested. The results show that dark incubated birds evinced no asymmetry in any measure while light incubated ones were right-eye dominant in both variables. However, light incubation induced a visual left hemispheric dominance by modulating two different processes, a left-hemispheric increase of visuoperceptual processes; and a right-hemispheric decrease for visuomotor speed. Taken together these data show that embryonic light stimulation elicits visual lateralization by differently modulating visuoperceptual and visuomotor systems in both hemispheres.

Asymmetrical modes of visual bottom-up and top-down integration in the thalamic nucleus rotundus of pigeons.

The aim of this study was to separate bottom-up and top-down influences within cerebral asymmetries. This was studied in the lateralized visual system of pigeons by recording from single units of the left and right diencephalic nucleus rotundus of the tectofugal pathway while visually stimulating the ipsilateral and/or contralateral eye. Analyses of response latencies revealed rotundal neurons with short and/or late response components. Cells with short latencies very likely represent bottom-up neurons participating in the ascending retinotectorotundal system. Because lidocaine injections into the visual Wulst produced a significant reduction of late response components only, neurons with long latencies were probably activated via a top-down telencephalotectorotundal system. The distribution and response characteristics of bottom-up and top-down neurons provided insight into several asymmetries of ascending and descending pathways. Asymmetries of the ascending retinotectorotundal system (bottom-up) were characterized by longer periods of tonic activation in the left and shorter response latencies in the right rotundus. Left-right differences in these responses probably facilitate faster access to visual input to the right hemisphere and a prolonged processing of this input in the left. The descending telencephalotectorotundal system (top-down) revealed a completely different lateralized organization. This system was characterized by long latency responses that exclusively derived from the left hemisphere, regardless of whether recordings took place in the left or the right rotundus. We assume that asymmetrical modes of visual processing within both hemispheres of the ascending tectofugal system are ultimately directed to left hemispheric forebrain mechanisms that subsequently generate executive control over sensory and motor structures.

Single unit activity during a Go/NoGo task in the prefrontal cortex of pigeons

Single unit activity was recorded during a delayed auditory/visual Go/NoGo task from the neostriatum caudolaterale (NCL) of pigeons, a multimodal associative avian forebrain structure comparable to the prefrontal cortex (PFC). The animals were trained to mandibulate (to open their beak) during the Go period after which they received a drop of water as reward. Neuronal activity changes were observed during the delay period (DELAY) between auditory and visual stimulation, to the onset of the visual stimulus or to the delivery of the reward. In some neurons, responses were related to the behavioral significance of the stimulus such that the neuronal activity was statistically different between Go and NoGo trials. Moreover, some units anticipated the upcoming reward or changed their firing frequency in a correlated manner prior to beak movements. These neuronal activity patterns suggest that the NCL provides a neural network that participates in the integration and processing of external stimuli in order to generate goal directed behavior.

Impaired learning of a color reversal task after NMDA receptor blockade in the pigeon (Columba livia) associative forebrain (neostriatum caudolaterale).

The neostriatum caudolaterale (NCL) in the pigeon (Columba livia) forebrain is a multisensory associative area and a functional equivalent to the mammalian prefrontal cortex (PFC). To investigate the role of N-methyl-D-aspartate (NMDA) receptors in the NCL for learning flexibility, the authors trained pigeons in a color reversal task while locally blocking NMDA receptors with D,L-2-2-amino-5-phosphonovalerate (AP-5). Controls received saline injections. AP-5-treated pigeons made significantly more errors and showed significantly stronger perseveration in a learning strategy applied by both groups but were unimpaired in initial learning. Results indicate that NMDA receptors in the NCL are necessary for efficient performance in this PFC-sensitive task, and that they are involved in extinction of obsolete information rather than in acquiring new information.

Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata).

There is considerable functional evidence implicating norepinephrine in modulating activity in the vocal control circuit of songbirds. However, our knowledge of noradrenergic inputs to the song system is incomplete. In this study, cholera toxin subunit B (CTB) injections into area X revealed projections from the noradrenergic nuclei locus coeruleus and subcoeruleus, and injections of biotinylated dextran amines into these noradrenergic nuclei labeled fibers in area X. The nonreciprocity of this connection was demonstrated by the absence of retrogradely labeled cells in area X following injections of CTB into the locus coeruleus. Additionally, we found novel inputs to area X from the nidopallium and arcopallium, the mesencephalic central gray, and the dorsolateralis anterior (DLL) and posterior (DLP) lateralis in the thalamus. Area X can be clearly distinguished from the surrounding medial striatum based on cytoarchitectural and chemical neuroanatomical criteria. We show here that neuromodulatory inputs to area X however, exhibit a considerable degree of overlap with the surrounding area. This finding suggests that regional specificity in neuromodulator action is most likely afforded by a specialization in receptor density and enzyme distribution rather than projections from the synthesizing nuclei. Our results extend current knowledge about noradrenergic projections to specialized nuclei of the song control circuit and provide neuroanatomical evidence for the functional action of norepinephrine‐modulating context‐dependent ZENK expression in area X. Furthermore, the novel projections to area X from telencephalic and thalamic areas could be new and interesting nodes in the striatopallidothalamic loop spanning the songbird brain. J. Comp. Neurol. 502:544–562, 2007.

Functional Aspects of Dopamine Metabolism in the Putative Prefrontal Cortex Analogue and Striatum of Pigeons (Columba livia)

Dopamine (DA) in mammalian associative structures, such as the prefrontal cortex (PFC), plays a prominent role in learning and memory processes, and its homeostasis differs from that of DA in the striatum, a sensorimotor region. The neostriatum caudolaterale (NCL) of birds resembles the mammalian PFC according to connectional, electrophysiological, and behavioral data. In the present study, DA regulation in the associative NCL and the striatal lobus parolfactorius (LPO) of pigeons was compared to uncover possible differences corresponding to those between mammalian PFC and striatum. Extracellular levels of DA and its metabolites (homovanillic acid [HVA], dihydroxyphenylacetic acid [DOPAC]) and the serotonin metabolite 5‐hydroxyindoleacetic acid (5‐HIAA) were investigated by in vivo microdialysis of urethane‐anesthetized pigeons under basal conditions and after systemic administration of D‐amphetamine. DA was reliably determined only in LPO dialysates, and DA metabolite levels were significantly higher in LPO than in NCL. The HVA/DOPAC ratio, indicating extracellular lifetime of DA, was more than twice as high in NCL than in LPO dialysates. After amphetamine, DA increased in LPO while still being undetectable in NCL, and DA metabolites decreased in both regions. 5‐HIAA slightly decreased in NCL dialysates. Amphetamine effects were delayed in NCL compared with the striatum. In conclusion, effects of amphetamine on the pigeons ascending monoamine systems resemble those found in mammals, suggesting similar regulatory properties. The neurochemical differences between NCL and LPO parallel those between associative regions, such as PFC and dorsal striatum in mammals. They may reflect weaker regulation of extracellular DA, favoring DAergic volume transmission, in associative than striatal forebrain regions. J. Comp. Neurol. 446:58–67, 2002.

Colocalization of Immediate Early Genes in Catecholamine Cells after Song Exposure in Female Zebra Finches (Taeniopygia guttata)

The physiological state of animals in many taxonomic groups can be modified via social interactions including simply receiving communication signals from conspecifics. Here, we explore whether the catecholaminergic system of female songbirds responds during social interactions that are limited to song reception. We measured the protein product of an immediate early gene (ZENK) within three catecholaminergic brain regions in song-exposed (n = 11) and silence-exposed (n = 6) female zebra finches (Taeniopygia guttata). ZENK-ir induction was quantified in catecholamine cells as well as within cells of unknown phenotypes in three brain regions that synthesize catecholamines, the ventral tegmental area, the periaqueductal gray and the locus coeruleus (LoC). Our results reveal that there are no significant differences in the overall number of cells expressing ZENK between song- and silence-exposed females. However, when we limited our measurements to catecholamine-containing cells, we noticed a greater number of catecholamine-containing cells expressing ZENK within the LoC in the song-exposed females compared to silence-exposed females. Furthermore, we measured five behaviors during the song- and silence-exposed period, as behavioral differences between these groups may account for differences in the coinduction of ZENK and TH-ir. Our results reveal that there were no statistically significant differences in the five measured behaviors between song- and silence-exposed females. Our study demonstrates that noradrenergic cells within the LoC are involved in the neural architecture underlying sound perception and that cells within the catecholaminergic system are modulated by social interactions, particularly the reception of signals used in animal communication.

Functional lateralization, interhemispheric transfer and position bias in serial reversal learning in pigeons (Columba livia)

Abstract In the present study we investigated lateralization of color reversal learning in pigeons. After monocular acquisition of a simple color discrimination with either the left or right eye, birds were tested in a serial reversal procedure. While there was only a slight and non-significant difference in choice accuracy during original color discrimination, a stable superiority of birds using the right eye emerged in serial reversals. Both groups showed a characteristic ‘learning-to-learn’ effect, but right-eyed subjects improved faster and reached a lower asymptotic error rate. Subsequent testing for interocular transfer demonstrated a difference between pre- and post-shift choice accuracy in pigeons switching from right to left eye but not vice versa. This can be accounted for by differences in maximum performance using either the left or right eye along with an equally efficient but incomplete interocular transfer in both directions. Detailed analysis of the birds’ response patterns during serial reversals revealed a preference for the right of two response keys in both groups. This bias was most pronounced at the beginning of a session. It decreased within sessions, but became more pronounced in late reversals, thus indicating a successful strategy for mastering the serial reversal task. Interocular transfer of response patterns revealed an unexpected asymmetry. Birds switching from right to left eye continued to prefer the right side, whereas pigeons shifting from left to right eye were now biased towards the left side. The results suggest that lateralized performance during reversal learning in pigeons rests on a complex interplay of learning about individual stimuli, stimulus dimensions, and lateralized response strategies.