Douglas R. Wylie

More on climbing fiber signals and their consequence(s)

The persistence of many contrasting notions of climbing fiber function after years of investigation testifies that the issue of climbing fiber contributions to cerebellar transactions is still unresolved. The proposed capabilities of the climbing fibers cover an impressive spectrum. For many researchers, the climbing fibers signal errors in motor performance, either in the conventional manner of frequency modulation or as a single announcement of an “unexpected event”. More controversial is the effect of these signals on the simple spike modulation of Purkinje cells. In some hands, they lead to a long-term depression of the strength of parallel fiber synapses, while, in other hands, they lead to a short-lasting enhancement of the responsiveness of Purkinje cells to mossy fiber inputs or contribute to the often-seen reciprocal relation between complex and simple spike modulation. For still other investigators, the climbing fibers serve internal timing functions through their capacity for synchronous and rhythmic firing. The above viewpoints are presented in the spirit of trying to reach some consensus about climbing fiber function. Each point of view is introduced by summarizing first the key observations made by the respective proponents; then the issues of short-lasting enhancement, reciprocity between complex and simple spikes, and synchrony and rhythmicity are addressed in the context of the visual climbing fiber system of the vestibulocerebellum.

Common reference frame for neural coding of translational and rotational optic flow.

Self-movement of an organism through the environment is guided jointly by information provided by the vestibular system and by visual pathways that are specialized for detecting ‘optic flow’,. Motion of any object through space, including the self-motion of organisms, can be described with reference to six degrees of freedom: rotation about three orthogonal axes, and translation along these axes. Here we describe neurons in the pigeon brain that respond best to optic flow resulting from translation along one of the three orthogonal axes. We show that these translational optic flow neurons, like rotational optic flow neurons, share a common spatial frame of reference with the semicircular canals of the vestibular system. The three axes to which these neurons respond best are the vertical axis and two horizontal axes orientated at 45° to either side of the body midline.

The processing of object and self-motion in the tectofugal and accessory optic pathways of birds

This paper reviews electrophysiological studies of motion processing in the tectofugal and accessory optic systems (AOS), and suggests these are specialized respectively for the analysis of object motion and self motion. Evidence is presented which shows that directionally specific neurons in the tectofugal system process local motion and are inhibited by wholefield motion. These cells respond to kinematograms and moving occlusion edges and may therefore also be involved in figure-ground segregation and depth perception. In contrast, cells in the nucleus of the basal optic root (nBOR), a component of the AOS, respond best to large slowly moving patterns. These cells are directionally selective preferring either upward, downward or backward directions. In the posterior region of the nBOR some cells have been found which are binocular and prefer either the same or opposite directions of motion in the two eyes. Thus, these cells are tuned to respond optimally to either translational or rotational components of wholefield motion and it is suggested these may be involved in the control of posture and locomotion.

The visual response properties of neurons in the nucleus of the basal optic root of the pigeon: a quantitative analysis

SummaryThe response characteristics of single-units in the nucleus of the basal optic root (nBOR) of the pigeon accessory optic system (AOS) were investigated using standard extracellular techniques. The receptive fields (RFs) were large (20–115° long) and elliptical and were found throughout the contralateral visual field with the exception of the red field. The RFs did not have inhibitory surrounds and there was no evidence of retinotopic organization. Most neurons responded to small moving spots although the optimal stimulus was wholefield motion of a particular direction. Analysis of 166 single-units showed that neurons preferring upward, downward and backward (nasal to temporal) motion were equally abundant (32.5, 32.5 and 31% respectively), while <5% preferred forward (temporal to nasal) motion. Mapping studies demonstrated that UP units were located in the dorsal portion of the nucleus; DOWN units were found ventral to UP units; BACK units were found along the ventral surface of the nucleus; and FORWARD units were found in the posterior-dorsolateral margin of the nucleus. Most cells were excited by wholefield motion in the preferred direction and inhibited by motion approximately 180° in the opposite direction, however, some cells lacked the excitatory component while others lacked the inhibitory component. Neurons were grouped into six categories based on the relative contributions of excitation and inhibition. These results are compared with investigations of the AOS of other vertebrates.

Projections of the Nucleus of the Basal Optic Root in Pigeons (Columba livia) Revealed With Biotinylated Dextran Amine

The nucleus of the basal optic root (nBOR) of the accessory optic system is known to be involved in the analysis of the visual consequences of self‐motion. Previous studies have shown that the nBOR in pigeons projects bilaterally to the vestibulocerebellum, the inferior olive, the interstitial nucleus of Cajal, and the oculomotor complex and projects unilaterally to the ipsilateral pretectal nucleus lentiformis mesencephali and the contralateral nBOR. By using the anterograde tracer biotinylated dextran amine, we confirmed these projections and found (previously unreported) projections to the nucleus Darkshewitsch, the nucleus ruber, the mesencephalic reticular formation, and the area ventralis of Tsai as well as ipsilateral projections to the central gray, the pontine nuclei, the cerebellar nuclei, the vestibular nuclei, the processus cerebellovestibularis, and the dorsolateral thalamus. In addition to previous studies, which showed a projection to the dorsomedial subdivision of the contralateral oculomotor complex, we found terminal labelling in the ventral and dorsolateral subdivisions.

A Dissociation of Motion and Spatial-Pattern Vision in the Avian Telencephalon: Implications for the Evolution of “Visual Streams”

The ectostriatum is a large visual structure in the avian telencephalon. Part of the tectofugal pathway, the ectostriatum receives a large ascending thalamic input from the nucleus rotundus, the homolog of the mammalian pulvinar complex. We investigated the effects of bilateral lesions of the ectostriatum in pigeons on visual motion and spatial-pattern perception tasks. To test motion perception, we measured performance on a task requiring detection of coherently moving random dots embedded in dynamic noise. To test spatial-pattern perception, we measured performance on the detection of a square wave grating embedded in static noise. A double dissociation was revealed. Pigeons with lesions to the caudal ectostriatum showed a performance deficit on the motion task but not the grating task. In contrast, pigeons with lesions to the rostral ectostriatum showed a performance deficit on the grating task but not the motion task. Thus, in the avian telencephalon, there is a separation of visual motion and spatial-pattern perception as there is in the mammalian telencephalon. However, this separation of function is in the targets of the tectofugal pathway in pigeons rather than in the thalamofugal pathway as described in mammals. The implications of these findings with respect to the evolution of the visual system are discussed. Specifically, we suggest that the principle of parallel visual streams originated in the tectofugal pathway rather than the thalamofugal pathway.

Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds

In mammals, species with more frontally oriented orbits have broader binocular visual fields and relatively larger visual regions in the brain. Here, we test whether a similar pattern of correlated evolution is present in birds. Using both conventional statistics and modern comparative methods, we tested whether the relative size of the Wulst and optic tectum (TeO) were significantly correlated with orbit orientation, binocular visual field width and eye size in birds using a large, multi-species data set. In addition, we tested whether relative Wulst and TeO volumes were correlated with axial length of the eye. The relative size of the Wulst was significantly correlated with orbit orientation and the width of the binocular field such that species with more frontal orbits and broader binocular fields have relatively large Wulst volumes. Relative TeO volume, however, was not significant correlated with either variable. In addition, both relative Wulst and TeO volume were weakly correlated with relative axial length of the eye, but these were not corroborated by independent contrasts. Overall, our results indicate that relative Wulst volume reflects orbit orientation and possibly binocular visual field, but not eye size.

Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus Lentiformis mesencephali.

Hummingbirds possess an array of morphological and physiological specializations that allow them hover such that they maintain a stable position in space for extended periods. Among birds, this sustained hovering is unique to hummingbirds, but possible neural specializations underlying this behavior have not been investigated. The optokinetic response (OKR) is one of several behaviors that facilitates stabilization. In birds, the OKR is generated by the nucleus of the basal optic root (nBOR) and pretectal nucleus lentiformis mesencephali (LM). Because stabilization during hovering is dependent on the OKR, we predicted that nBOR and LM would be significantly enlarged in hummingbirds. We examined the relative size of nBOR, LM, and other visual nuclei of 37 species of birds from 13 orders, including nine hummingbird species. Also included were three species that hover for short periods of time (transient hoverers; a kingfisher, a kestrel, and a nectarivorous songbird). Our results demonstrate that, relative to brain volume, LM is significantly hypertrophied in hummingbirds compared with other birds. In the transient hoverers, there is a moderate enlargement of the LM, but not to the extent found in the hummingbirds. The same degree of hypertrophy is not, however, present in nBOR or the other visual nuclei measured: nucleus geniculatus lateralis, pars ventralis, and optic tectum. This selective hypertrophy of LM and not other visual nuclei suggests that the direction‐selective optokinetic neurons in LM are critical for sustained hovering flight because of their prominent role in the OKR and gaze stabilization. J. Comp. Neurol. 500:211–221, 2007.

Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow

Previous electrophysiological studies have shown that neurons in the nucleus of the basal optic root (nBOR) of the pigeon respond best to wholefield stimuli moving slowly in a particular direction in the contralateral visual field. In this study, we have found that some nBOR neurons respond to wholefield stimulation of both eyes. These binocular neurons have spatially separate receptive fields in both visual fields. Some binocular neurons prefer the same direction of wholefield motion in both eyes, and thus respond best to wholefield visual motion which would result from translation movements of the bird, either ascent, descent, or forward and backward motion. Other neurons prefer opposite directions of wholefield motion in each eye and therefore respond optimally to wholefield visual motion simulating rotational movements of the bird, either roll or yaw. These binocular neurons may play a crucial part in the locomotor behavior of the pigeon by providing visual information distinguishing translational and rotational movements.

Purkinje Cell Compartmentation as Revealed by Zebrin II Expression in the Cerebellar Cortex of Pigeons (Columba livia)

Purkinje cells in the cerebellum express the antigen zebrin II (aldolase C) in many vertebrates. In mammals, zebrin is expressed in a parasagittal fashion, with alternating immunopositive and immunonegative stripes. Whether a similar pattern is expressed in birds is unknown. Here we present the first investigation into zebrin II expression in a bird: the adult pigeon (Columba livia). Western blotting of pigeon cerebellar homogenates reveals a single polypeptide with an apparent molecular weight of 36 kDa that is indistinguishable from zebrin II in the mouse. Zebrin II expression in the pigeon cerebellum is prominent in Purkinje cells, including their dendrites, somata, axons, and axon terminals. Parasagittal stripes were apparent with bands of Purkinje cells that strongly expressed zebrin II (+ve) alternating with bands that expressed zebrin II weakly or not at all (−ve). The stripes were most prominent in folium IXcd, where there were seven +ve/−ve stripes, bilaterally. In folia VI–IXab, several thin stripes were observed spanning the mediolateral extent of the folia, including three pairs of +ve/−ve stripes that extended across the lateral surface of the cerebellum. In folium VI the zebrin II expression in Purkinje cells was stronger overall, resulting in less apparent stripes. In folia II–V, four distinct +ve/−ve stripes were apparent. Finally, in folia I (lingula) and X (nodulus) all Purkinje cells strongly expressed zebrin II. These data are compared with studies of zebrin II expression in other species, as well as physiological and neuroanatomical studies that address the parasagittal organization of the pigeon cerebellum. J. Comp. Neurol. 501:619–630, 2007.