Nathan A. Crowder

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.

Saccadic modulation of neural responses: possible roles in saccadic suppression, enhancement, and time compression.

Humans use saccadic eye movements to make frequent gaze changes, yet the associated full-field image motion is not perceived. The theory of saccadic suppression has been proposed to account for this phenomenon, but it is not clear whether suppression originates from a retinal signal at saccade onset or from the brain before saccade onset. Perceptually, visual sensitivity is reduced before saccades and enhanced afterward. Over the same time period, the perception of time is compressed and even inverted. We explore the origins and neural basis of these effects by recording from neurons in the dorsal medial superior temporal area (MSTd) of alert macaque monkeys. Neuronal responses to flashed presentations of a textured pattern presented at random times relative to saccades exhibit a stereotypical pattern of modulation. Response amplitudes are strongly suppressed for flashes presented up to 90 ms before saccades. Immediately after the suppression, there is a period of 200–450 ms in which flashes generate enhanced response amplitudes. Our results show that (1) MSTd is not directly suppressed, rather suppression is inherited from earlier visual areas; (2) early suppression of the visual system must be of extra-retinal origin; (3) postsaccadic enhancement of neural activity occurs in MSTd; and (4) the enhanced responses have reduced latencies. As a whole, these observations reveal response properties that could account for perceptual observations relating to presaccadic suppression, postsaccadic enhancement and time compression.

Retinal Anatomy and Visual Performance in a Diurnal Cone-Rich Laboratory Rodent, the Nile Grass Rat (Arvicanthis niloticus)

Unlike laboratory rats and mice, muridae of the Arvicanthis family (A. ansorgei and A. niloticus) are adapted to functioning best in daylight. To date, they have been used as experimental models mainly in studies of circadian rhythms. However, recent work aimed at optimizing photoreceptor‐directed gene delivery vectors (Khani et al. [ 2007 ] Invest Ophthalmol Vis Sci 48:3954–3961) suggests their potential usefulness for studying retinal pathologies and therapies. In the present study we analyzed the retinal anatomy and visual performance of the Nile grass rat (A. niloticus) using immunohistofluorescence and the optokinetic response (OKR). We found that ≈35–40% of photoreceptors are cones; that many neural features of the inner retina are similar to those in other diurnal mammals; and that spatial acuity, measured by the OKR, is more than two times that of the usual laboratory rodents. These observations are consistent with the known diurnal habits of this animal, and further support its pertinence as a complementary model for studies of structure, function, and pathology in cone‐rich mammalian retinae. J. Comp. Neurol. 510:525–538, 2008.

Topographic Organization of Inferior Olive Cells Projecting to Translational Zones in the Vestibulocerebellum of Pigeons

In the nodulus and ventral uvula of pigeons, there are four parasagittal zones containing Purkinje cells responsive to patterns of optic flow that results from self‐translation along a particular axis in three‐dimensional space. By using a three‐axis system to describe the preferred direction of translational optic flow, where +X, +Y, and +Z represent rightward, upward, and forward self‐motion, respectively, the four cell types are: +Y, −Y, −X−Z, and −X+Z (assuming recording from the left side of the head). The −X−Z zone is the most medial, followed in sequence by the −X+Z, −Y zone, and the +Y zones. In this study, we injected the retrograde tracer cholera toxin subunit B into each of the four translational zones to determine the origin of the climbing fiber inputs in the inferior olive. Retrograde labeling in the inferior olive was found in the ventrolateral margin of the medial column from injections into all four translational zones; however, there was a clear functional topography. Retrograde labeling from −Y zone injections was found most rostrally in the medial column, whereas retrogradely labeled cells from −X−Z zone injections were found most caudally in the medial column. Labeling from +Y and −X+Z zone injections were found between the labeling from −Y zones and −X−Z zones, with +Y labeling located slightly caudal to −X+Z labeling. J. Comp. Neurol. 419:87–95, 2000.

Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus

Previous neurophysiologic research in birds and mammals has shown that there are two types of Purkinje cells in the flocculus. The first type shows maximal modulation in response to rotational optokinetic stimulation about the vertical axis (rVA neurons). The second type shows maximal modulation in response to rotational optokinetic stimulation about a horizontal axis oriented 45 degrees to contralateral azimuth (rH45c neurons). In pigeons, the rVA and rH45c are organized into four alternating parasagittal zones. In this study we investigated the projections of Purkinje cells in the rVA and rH45c zones by using the anterograde tracers biotinylated dextran amine and cholera toxin subunit B. After iontophoretic injections of tracers into the rH45c zones, heavy anterograde labeling was found in the infracerebellar nucleus and the medial margin of the superior vestibular nucleus. Some labeling was also consistently observed in the lateral cerebellar nucleus and the dorsolateral vestibular nucleus. After injections into the rVA zones, heavy anterograde labeling was found in the medial and descending vestibular nuclei, the nucleus prepositus hypoglossi, and the central region of the superior vestibular nucleus. Less labeling was seen in the tangential nucleus, the dorsolateral vestibular nucleus, and the lateral vestibular nucleus, pars ventralis. These results are compared and contrasted with findings in mammalian species. J. Comp. Neurol. 456:140–153, 2003.

Characterizing contrast adaptation in a population of cat primary visual cortical neurons using Fisher information

When cat V1/V2 cells are adapted to contrast at their optimal orientation, a reduction in gain and/or a shift in the contrast response function is found. We investigated how these factors combine at the population level to affect the accuracy for detecting variations in contrast. Using the contrast response function parameters from a physiologically measured population, we model the population accuracy (using Fisher information) for contrast discrimination. Adaptation at 16%, 32%, and 100% contrast causes a shift in peak accuracy. Despite an overall drop in firing rate over the whole population, accuracy is enhanced around the adapted contrast and at higher contrasts, leading to greater efficiency of contrast coding at these levels. The estimated contrast discrimination threshold curve becomes elevated and shifted toward higher contrasts after adaptation, as has been found previously in human psychophysical experiments.

Influence of adapting speed on speed and contrast coding in the primary visual cortex of the cat.

Adaptation is a ubiquitous property of the visual system. Adaptation often improves the ability to discriminate between stimuli and increases the operating range of the system, but is also associated with a reduced ability to veridically code stimulus attributes. Adaptation to luminance levels, contrast, orientation, direction and spatial frequency has been studied extensively, but knowledge about adaptation to image speed is less well understood. Here we examined how the speed tuning of neurons in cat primary visual cortex was altered after adaptation to speeds that were slow, optimal, or fast relative to each neurons speed response function. We found that the preferred speed (defined as the speed eliciting the peak firing rate) of the neurons following adaptation was dependent on the speed at which they were adapted. At the population level cells showed decreases in preferred speed following adaptation to speeds at or above the non‐adapted speed, but the preferred speed did not change following adaptation to speeds lower than the non‐adapted peak. Almost all cells showed response gain control (reductions in absolute firing capacity) following speed adaptation. We also investigated the speed dependence of contrast adaptation and found that most cells showed contrast gain control (rightward shifts of their contrast response functions) and response gain control following adaptation at any speed. We conclude that contrast adaptation may produce the response gain control associated with speed adaptation, but shifts in preferred speed require an additional level of processing beyond contrast adaptation. A simple model is presented that is able to capture most of the findings.

Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus

Previous electrophysiological studies in pigeons have shown that the complex spike activity of Purkinje cells in the medial vestibulocerebellum (nodulus and ventral uvula) is modulated by patterns of optic flow that result from self‐translation along a particular axis in three‐dimensional space. There are four response types based on the axis of preferred translational optic flow. By using a three axis system, where +X, +Y, and +Z represent rightward, upward, and forward self‐motion, respectively, the four cell types are t(+Y), t(–Y), t(–X–Z), and t(–X+Z), with the assumption of recording from the left side of the head. These response types are organized into parasagittal zones. In this study, we injected the anterograde tracer biotinylated dextran amine into physiologically identified zones. The t(–X–Z) zone projected dorsally within the vestibulocerebellar process (pcv) on the border with the medial cerebellar nucleus (CbM), and labeling was found in the CbM itself. The t(–X+Z) zone also projected to the pcv and CbM, but to areas ventral to the projection sites of the t(–X–Z) zone. The t(–Y) zone also projected to the pcv, but more ventrally on the border with the superior vestibular nucleus (VeS). Some labeling was also found in the dorsal VeS and the dorsolateral margin of the caudal descending vestibular nucleus, and a small amount of labeling was found laterally in the caudal margin of the medial vestibular nucleus. The data set was insufficient to draw conclusions about the projection of the t(+Y) zone. These results are contrasted with the projections of the flocculus, compared with the primary vestibular projection, and implications for collimotor function are discussed. J. Comp. Neurol. 465:179–194, 2003.

Neural basis of time changes during saccades

This work was made possible through collaboration with M. Mustari and S. Ono at the Yerkes National Primate Research Centre, Atlanta, USA, where the monkey recordings were conducted. Funding came from the Australian Research Council Centre for Excellence in Vision Science, an ARC linkage grant and from the NIH.

Dynamic contrast change produces rapid gain control in visual cortex

During normal vision, objects moving in the environment, our own body movements and our eye movements ensure that the receptive fields of visual neurons are being presented with continually changing contrasts. Thus, the visual input during normal behaviour differs from the type of stimuli traditionally used to study contrast coding, which are presented in a step‐like manner with abrupt changes in contrast followed by prolonged exposure to a constant stimulus. The abrupt changes in contrast typically elicit brief periods of intense firing with low variability called onset transients. Onset transients provide the visual system with a powerful and reliable cue that the visual input has changed. In this paper we investigate visual processing in the primary visual cortex of cats in response to stimuli that change contrast dynamically. We show that 1–4 s presentations of dynamic increases and decreases in contrast can generate stronger contrast gain control than several minutes exposure to a stimulus of constant contrast. Thus, transient mechanisms of contrast coding are not only less variable than sustained responses but are also more rapid and flexible. Finally, we propose a quantitative model of contrast coding which accounts for changes in spike rate over time in response to dynamically changing image contrast.