Asymmetric top-down modulation of ascending visual pathways in pigeons.

Cerebral asymmetries are a ubiquitous phenomenon evident in many species, incl. humans, and they display some similarities in their organization across vertebrates. In many species the left hemisphere is associated with the ability to categorize objects based on abstract or experience-based behaviors. Using the asymmetrically organized visual system of pigeons as an animal model, we show that descending forebrain pathways asymmetrically modulate visually evoked responses of single thalamic units. Activity patterns of neurons within the nucleus rotundus, the largest thalamic visual relay structure in birds, were differently modulated by left and right hemispheric descending systems. Thus, visual information ascending towards the left hemisphere was modulated by forebrain top-down systems at thalamic level, while right thalamic units were strikingly less modulated. This asymmetry of top-down control could promote experience-based processes within the left hemisphere, while biasing the right side towards stimulus-bound response patterns. In a subsequent behavioral task we tested the possible functional impact of this asymmetry. Under monocular conditions, pigeons learned to discriminate color pairs, so that each hemisphere was trained on one specific discrimination. Afterwards the animals were presented with stimuli that put the hemispheres in conflict. Response patterns on the conflicting stimuli revealed a clear dominance of the left hemisphere. Transient inactivation of left hemispheric top-down control reduced this dominance while inactivation of right hemispheric top-down control had no effect on response patterns. Functional asymmetries of descending systems that modify visual ascending pathways seem to play an important role in the superiority of the left hemisphere in experience-based visual tasks.

Lateralized reward-related visual discrimination in the avian entopallium.

In humans and many other animals, the two cerebral hemispheres are partly specialized for different functions. However, knowledge about the neuronal basis of lateralization is mostly lacking. The visual system of birds is an excellent model in which to investigate hemispheric asymmetries as birds show a pronounced left hemispheric advantage in the discrimination of various visual objects. In addition, visual input crosses at the optic chiasm and thus testing of each hemisphere is easily accomplished. We aimed to find a neuronal correlate for three hallmarks of visual lateralization in pigeons: first, the animals learn faster with the right eye-left hemisphere; second, they reach higher performance levels under this condition; third, visually guided behavior is mostly under left hemisphere control. To this end, we recorded from the left and right forebrain entopallium while the animals performed a colour discrimination task. We found that, even before learning, left entopallial neurons were more responsive to visual stimulation. Subsequent discrimination acquisition recruited more neuronal responses in the left entopallium and these cells showed a higher degree of differentiation between the rewarded and the unrewarded stimulus. Thus, differential left-right responses are already present, albeit to a modest degree, before learning. As soon as some cues are associated with reward, however, this asymmetry increases substantially and the higher discrimination ratio of the left hemispheric tectofugal pathway would not only contribute to a higher performance of this hemisphere but could thereby also result in a left hemispheric dominance over downstream motor structures via reward-associated feedback systems.

Neuronal encoding of meaning: establishing category-selective response patterns in the avian 'prefrontal cortex'.

Forebrain association areas interweave perceived stimuli with acquired representations of own actions and their outcome. Often, relevant stimuli come in a bewildering variety of shapes and sizes and we slowly have to learn to group them into meaningful categories. Therefore, the aim of the present study was twofold: First, to reveal how single units in the pigeon's nidopallium caudolaterale (NCL), a functional analogue of the mammalian prefrontal cortex (PFC), encode stimuli that differ in visual features but not in behavioral relevance. The second aim was to understand how these categorical representations are established during learning. Recordings were made from NCL neurons while pigeons performed a go-nogo categorization paradigm. Responses during presentation of the two S+ stimuli and non-responding during presentation of the two S- stimuli were followed by reward. We recorded from two pigeons at different learning stages. In the beginning of the learning process, neurons were active during and shortly before reward, but only in go trials. These data suggest that during the early phase of learning avian 'prefrontal' neurons code for rewards associated with the same behavioral demand, while ignoring feature differences of stimuli within one category. When learning progressed, (1) category selectivity became stronger, (2) responses selective for nogo stimuli appeared, and (3) reward-related responses disappeared in favor of category-selective responses during the stimulus phase. This backward shift in time resembles response patterns assumed by the temporal difference (TD) model of reinforcement learning, but goes beyond it, since it reflects the neuronal correlate of functional categories.

Insight without cortex: lessons from the avian brain.

Insight is a cognitive feature that is usually regarded as being generated by the neocortex and being present only in humans and possibly some closely related primates. In this essay we show that especially corvids display behavioral skills within the domains of object permanence, episodic memory, theory of mind, and tool use/causal reasoning that are insightful. These similarities between humans and corvids at the behavioral level are probably the result of a convergent evolution. Similarly, the telencephalic structures involved in higher cognitive functions in both species show a high degree of similarity, although the forebrain of birds has no cortex-like lamination. The neural substrate for insight-related cognitive functions in mammals and birds is thus not necessarily based on a laminated cortical structure but can be generated by differently organized forebrains. Hence, neither is insight restricted to mammals, as predicted from a "scala naturae", nor is the laminated cortex a prerequisite for the highest cognitive functions.

Grouping of artificial objects in pigeons: an inquiry into the cognitive architecture of an avian mind.

How does a pigeon see the world? Although pigeons are known to be adept at learning large numbers of figures, colors, and natural images, various experiments show that their visual cognitive specialization is more geared towards seeing colors and textures instead of shapes. They also excel in the analysis of local features instead of shapes that can only be differentiated by their outline. We therefore embarked into a detailed analysis of the relative weight of colors versus shapes in an object grouping task. At the same time we used a design that gave us information on the question of the relative importance of the S+ and S- in cognitive tests. Our strategy was to use the classic matching to sample task in which pigeons have to associate a sample with another stimulus (S+), which belongs to the same arbitrary group while at the same time avoiding choosing another stimulus (S-), which is part of another arbitrary group. Our results clearly reveal that color is, relative to shape, the primary cue that pigeons use to guide their decisions. Although they are in principle able to use shape information, they utilize shape as the last cognitive resort. Our data further reveal that pigeons guide their decisions in a matching to sample task primarily by focusing on the S+, although they also utilize information from the S-, albeit to a smaller extent. They are flexibly able to use cognitive match- or nonmatch-strategies depending on the presence or absence of color- or shape-cues.

Visual responses and afferent connections of the n. ventrolateralis thalami (VLT) in the pigeon (Columba livia).

The nucleus ventrolateralis thalami (VLT) in pigeons receives direct retinal and forebrain projections and has reciprocal connections with the optic tectum. Although VLT is a component of the avian visual system, no study directly examined its connections or its cellular response characteristics. We, therefore, recorded from single units in the pigeon's VLT while visually stimulating the ipsi- and/or contralateral eye. In addition, tracing experiments were conducted to investigate its afferent connections. Electrophysiologically, we discovered three types of neurons, two of which were probably activated via a top-down telencephalotectal system (latencies > 100 ms). Type I neurons responded to uni- and bilateral and type II neurons exclusively to bilateral stimulation. Type III neurons were probably activated by retinal or retinotectal input (latencies < 27 ms) and responded to contra- and bilateral stimulation. Retrograde tracer injections into the VLT revealed an ipsilateral forebrain input from the visual Wulst, from subregions of the arcopallium, and bilateral afferents from the optic tectum. Most intriguing was the direct connection between the VLTs of both hemispheres. We suggest that the avian VLT is part of a system that integrates visuomotor processes which are controlled by both forebrain hemispheres and that VLT contributes to descending tectomotor mechanisms.

Neuronal synchronicity in the pigeon "prefrontal cortex" during learning.

In general electrophysiological studies focus on the investigation of changes in discharge rate of neuronal responses which are related to sensory or behavioral events. However, equally important for explanation of higher cognitive functions, learning, memory storage and complex behavior is the interaction between neurons that are connected in cell assemblies. Synchronized inputs onto a neuron are much more effective at eliciting the following activity than uncorrelated inputs. The goal of the present study was to determine either the changes in discharge rate of neurons in the pigeon nidopallium caudolaterale as well as the synchronicity of these neurons during a discriminatory learning task. We found rate modulation effects as well as modulation of synchronization during the learning process.

Responses of diencephalic neurons to sensory stimulation in the goldfish, Carassius auratus.

We studied the responses to sensory stimulation in two diencephalic areas, the central posterior nucleus of the dorsal thalamus (CP) and the anterior tuberal nucleus of the hypothalamus (TA). In both the CP and the TA, units sensitive to acoustic (500-Hz sound), hydrodynamic (25-Hz dipole stimulus), and visual (640-nm light flash) stimuli were found. In the CP, most units were unimodal and responded exclusively to visual stimulation. In contrast, in the TA, most units responded to more than one modality. The data suggest that the CP is primarily involved in the unimodal processing of sensory information, whereas the TA may be involved in multisensory integration.

Response properties of diencephalic neurons to visual, acoustic and hydrodynamic stimulation in the goldfish, Carassius auratus.

We studied the responses to sensory stimulation of three diencephalic areas, the central posterior nucleus of the dorsal thalamus, the anterior tuberal nucleus of the hypothalamus, and the preglomerular complex. Units sensitive to acoustic (500 Hz tone burst), hydrodynamic (25 Hz dipole stimulus) and visual (640 nm light flash) stimuli were found in both the central posterior and anterior tuberal nucleus. In contrast, unit responses or large robust evoked potentials confined to the preglomerular complex were not found. In the central posterior nucleus, most units were unimodal. Many units responded exclusively to visual stimulation and exhibited a variety of temporal response patterns to light stimuli. In the anterior tuberal nucleus of the hypothalamus, most units responded to more than one modality and showed a stronger response decrement to stimulus repetitions than units in the central posterior nucleus. Our data suggest that units in the central posterior nucleus are primarily involved in the unimodal processing of sensory information whereas units in the anterior tuberal nucleus of the hypothalamus may be involved in multisensory integration.