scholarly journals Temporal Frequency and Velocity-Like Tuning in the Pigeon Accessory Optic System

2003 ◽  
Vol 90 (3) ◽  
pp. 1829-1841 ◽  
Author(s):  
Nathan A. Crowder ◽  
Michael R.W. Dawson ◽  
Douglas R.W. Wylie

Neurons in the accessory optic system (AOS) and pretectum are involved in the analysis of optic flow and the generation of the optokinetic response. Previous studies found that neurons in the pretectum and AOS exhibit direction selectivity in response to large-field motion and are tuned in the spatiotemporal domain. Furthermore, it has been emphasized that pretectal and AOS neurons are tuned to a particular temporal frequency, consistent with the “correlation” model of motion detection. We examined the responses of neurons in the nucleus of the basal optic root (nBOR) of the AOS in pigeons to large-field drifting sine wave gratings of varying spatial (SF) and temporal frequencies (TF). nBOR neurons clustered into two categories: “Fast” neurons preferred low SFs and high TFs, and “Slow” neurons preferred high SFs and low TFs. The fast neurons were tuned for TF, but the slow nBOR neurons had spatiotemporally oriented peaks that suggested velocity tuning (TF/SF). However, the peak response was not independent of SF; thus we refer to the tuning as “apparent velocity tuning” or “velocity-like tuning.” Some neurons showed peaks in both the fast and slow regions. These neurons were TF-tuned at low SFs, and showed velocity-like tuning at high SFs. We used computer simulations of the response of an elaborated Reichardt detector to show that both the TF-tuning and velocity-like tuning shown by the fast and slow neurons, respectively, may be explained by modified versions of the correlation model of motion detection.

2004 ◽  
Vol 91 (1) ◽  
pp. 274-285 ◽  
Author(s):  
Nathan A. Crowder ◽  
Clayton T. Dickson ◽  
Douglas R.W. Wylie

The pretectal nucleus lentiformis mesencephali (LM) and the nucleus of the basal optic root (nBOR) of the avian accessory optic system (AOS) are retinal-recipient visual nuclei involved in the analysis of optic flow that results from self-motion, and in the generation of the optokinetic response. Neurons in these nuclei show direction selectivity in response to large-field motion and are tuned in the spatiotemporal domain. In addition to retinal afferentation, both the nBOR and LM receive afferents from the Wulst, which is thought to be the avian homolog of the primary visual cortex. We examined the effects of Wulst electrical stimulation on the activity of LM neurons and recorded the directional and spatiotemporal tuning of LM neurons in pigeons before, during, and after the Wulst was temporarily inactivated by lidocaine injection. In response to Wulst electrical stimulation, LM neurons showed either short-latency excitation followed by longer-latency inhibition (W+ cells), or only a longer-latency inhibition (W– cells). The average response latencies for W+ and W– cells were 13.5 and 28.3 ms, respectively. The effects of Wulst stimulation did not correlate with either the directional or spatiotemporal tuning of the LM neurons. Injection of lidocaine into the nBOR reduced the longer-latency oscillations of W+ and W– cells. When the Wulst was temporarily inactivated by lidocaine neither the directional nor spatiotemporal response properties of LM neurons were affected. The possible functions of the projection from the Wulst to the LM are discussed.


2003 ◽  
Vol 90 (2) ◽  
pp. 1140-1151 ◽  
Author(s):  
Nathan A. Crowder ◽  
Hugo Lehmann ◽  
Marise B. Parent ◽  
Douglas R.W. Wylie

The nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) and the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion and are important for oculomotor control. These neurons have large receptive fields and exhibit direction selectivity to large moving stimuli. In response to drifting sine wave gratings, LM and nBOR neurons are tuned to either low spatial/high temporal frequencies (SF, TF) or high SF/low TF stimuli. Given that velocity = TF/SF, these are referred to as “fast” and “slow” neurons, respectively. There is a heavy projection from the AOS to the pretectum, although its function is unknown. We recorded the directional and spatio-temporal tuning of LM units in pigeons before and after nBOR was inactivated by tetrodotoxin injection. After nBOR inactivation, changes in direction preference were observed for only one of 18 LM units. In contrast, the spatio-temporal tuning of LM units was dramatically altered by nBOR inactivation. Two major effects were observed. First, in response to motion in the preferred direction, most (82%) neurons showed a substantially reduced (μ = –67%) excitation to low SF/high TF gratings. Second, in response to motion in the anti-preferred direction, most (63%) neurons showed a dramatically reduced (μ = –78%) inhibition to high SF/low TF gratings. Thus the projection from the nBOR contributes to the spatio-temporal tuning rather than the directional tuning of LM neurons. We propose a descriptive model whereby LM receives inhibitory and excitatory input from “slow” and “fast” nBOR neurons, respectively.


2000 ◽  
Vol 84 (5) ◽  
pp. 2529-2540 ◽  
Author(s):  
Douglas R. W. Wylie ◽  
Nathan A. Crowder

Neurons in the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion. Previous studies have shown that LM neurons have large receptive fields in the contralateral eye, are excited in response to largefield stimuli moving in a particular (preferred) direction, and are inhibited in response to motion in the opposite (anti-preferred) direction. We investigated the responses of LM neurons to sine wave gratings of varying spatial and temporal frequency drifting in the preferred and anti-preferred directions. The LM neurons fell into two categories. “Fast” neurons were maximally excited by gratings of low spatial [0.03–0.25 cycles/° (cpd)] and mid-high temporal frequencies (0.5–16 Hz). “Slow” neurons were maximally excited by gratings of high spatial (0.35–2 cpd) and low-mid temporal frequencies (0.125–2 Hz). Of the slow neurons, all but one preferred forward (temporal to nasal) motion. The fast group included neurons that preferred forward, backward, upward, and downward motion. For most cells (81%), the spatial and temporal frequency that elicited maximal excitation to motion in the preferred direction did not coincide with the spatial and temporal frequency that elicited maximal inhibition to gratings moving in the anti-preferred direction. With respect to motion in the anti-preferred direction, a substantial proportion of the LM neurons (32%) showed bi-directional responses. That is, the spatiotemporal plots contained domains of excitation in addition to the region of inhibition. Neurons tuned to stimulus velocity across different spatial frequency were rare (5%), but some neurons (39%) were tuned to temporal frequency. These results are discussed in relation to previous studies of the responses of neurons in the accessory optic system and pretectum to drifting gratings and other largefield stimuli.


1988 ◽  
Vol 60 (6) ◽  
pp. 2055-2072 ◽  
Author(s):  
J. I. Simpson ◽  
C. S. Leonard ◽  
R. E. Soodak

1. To compare the spatial organization of the direction selectivity of neurons in the medial terminal nucleus (MTN) of the accessory optic system with that of neurons in the adjacent ventral tegmentum, extracellular single-unit recordings were made in the anesthetized rabbit. The ventral tegmental neurons were located in a region called the visual tegmental relay zone (VTRZ), which is defined by the ventral tegmental terminal field of contralaterally projecting MTN neurons. 2. Some of the present sample of MTN neurons (5 of 34) had monocular receptive fields composed of two parts distinguished by a marked difference in the orientation of their respective direction-selective tuning curves. For one part of the receptive field the preferred excitatory direction was "up," while for the other part it was "down." Such receptive fields for one eye were called bipartite, whereas the more usually encountered MTN receptive fields, which could be characterized by a single direction-selective tuning curve, were called uniform. 3. Of the 16 neurons recorded from the VTRZ, all but one were binocular. For these neurons, both uniform and bipartite receptive fields were found for each eye alone. The only monocular neuron encountered in the VTRZ had a contralateral, bipartite receptive field. 4. The spatial organization of the direction selectivity of bipartite receptive fields strongly suggests that they are suited to represent rotation of the visual field about a horizontal axis located in the vertical plane that divides the receptive field into two parts. 5. The boundary between the two parts of the bipartite receptive fields was found using handheld visual stimuli at one of two azimuthal locations, either close to 45 degrees or between 95 and 125 degrees (the 0 degree reference was rostral in the midsagittal plane). This particular structure of the bipartite receptive fields suggests that their preferred rotation axes have a close spatial relation to the best-response axes of the semicircular canals. 6. Seven VTRZ neurons were antidromically activated by electrical stimulation of the ipsilateral dorsal cap of the inferior olive. Since the receptive fields of VTRZ neurons have many of the structural features characteristic of the receptive fields of rostral dorsal cap neurons we conclude that the spatial organization of the receptive fields of dorsal cap neurons is, for the most part, synthesized prior to the inferior olive.(ABSTRACT TRUNCATED AT 400 WORDS)


1996 ◽  
Vol 13 (2) ◽  
pp. 375-383 ◽  
Author(s):  
Alexander F. Rosenberg ◽  
Michael Ariel

AbstractThe turtle's optokinetic response is described by a simple model that incorporates visual-response properties of neurons in the pretectum and accessory optic system. Using data from neuronal and eye-movement recordings that have been previously published, the model was realized using algebraic-block simulation software. It was found that the optokinetic response, modelled as a simple negative feedback system, was similar to that measured from a behaving animal. Because the responses of retinal-slip detecting neurons corresponded to the nonlinear, closed-loop optokinetic response, it was concluded that the visual signals encoded in these neurons could provide sufficient sensory information to drive the optokinetic reflex. Furthermore, it appears that the low gain of optokinetic eye movements in turtles, which have a negligible velocity storage time constant, may allow stable oculomotor output in spite of neuronal delays in the reflex pathway. This model illustrates how visual neurons in the pretectum and accessory optic system can contribute to visually guided eye movements.


2005 ◽  
Vol 93 (3) ◽  
pp. 1266-1277 ◽  
Author(s):  
Ian R. Winship ◽  
Peter L. Hurd ◽  
Douglas R. W. Wylie

The pretectum, accessory optic system (AOS), and vestibulocerebellum (VbC) have been implicated in the analysis of optic flow and generation of the optokinetic response. Recently, using drifting sine-wave gratings as stimuli, it has been shown that pretectal and AOS neurons exhibit spatiotemporal tuning. In this respect, there are two groups: fast neurons, which prefer low spatial frequency (SF) and high temporal frequency (TF) gratings, and slow neurons, which prefer high SF–low TF gratings. In pigeons, there are two pathways from the pretectum and AOS to the VbC: a climbing fiber (CF) pathway to Purkinje cells (P cells) via the inferior olive and a direct mossy fiber (MF) pathway to the granular layer (GL). In the present study, we assessed spatiotemporal tuning in the VbC of ketamine-anesthetized pigeons using standard extracellular techniques. Recordings were made from 17 optic-flow-sensitive units in the GL, presumably granule cells or MF rosettes, and the complex spike activity (CSA) of 39 P-cells, which reflects CF input. Based on spatiotemporal tuning to gratings moving in the preferred direction, eight GL units were classified as fast units, with a primary response to low SF–high TF gratings (mean = 0.13 cpd/8.24 Hz), whereas nine were slow units preferring high SF–low TF gratings (mean = 0.68 cpd/0.30 Hz). CSA was almost exclusively tuned to slow gratings (mean = 0.67 cpd/0.35 Hz). We conclude that MF input to the VbC is from both fast and slow cells in the AOS and pretectum, whereas the CF input is primarily tuned to slow gratings.


1984 ◽  
Vol 51 (2) ◽  
pp. 276-293 ◽  
Author(s):  
K. L. Grasse ◽  
M. S. Cynader

Visual responses were examined quantitatively in 96 units in the lateral (LTN) and dorsal (DTN) terminal nuclei of the cat accessory optic system (AOS). The receptive fields of LTN and DTN cells were quite large, with an average diameter of approximately 60 degrees. Individual cell receptive fields, which could be as small as 30 degrees vertically by 15 degrees horizontally or as large as 100 by 100 degrees, always included the area centralis. Large, moving textured stimuli provoked optimal modulation in these cells. In response to a 100 by 80 degrees random-dot pattern moving at a constant velocity, nearly all cells in both the LTN and DTN displayed a high degree of direction selectivity. Directional response profiles were subjected to a vector analysis that generated two quantities proportional to the direction and magnitude of the major excitatory (E vectors) and inhibitory (I vectors) responses of individual cells. Directional vectors of the LTN displayed a strikingly bimodal distribution: E vectors of individual LTN cells pointed either upward (25 of 49) or downward (23 of 49). I vectors also pointed either up or down in a direction opposite to that of the E vector for the same cell. E and I vectors in both LTN and DTN units were separated by approximately 180 degrees. With few exceptions, E vectors of DTN cells pointed in a horizontal-medial direction, while DTN I vectors pointed in a horizontal-lateral direction. A relatively broad range of stimulus velocities (0.8-102.4 degrees/s) evoked maximal excitation in individual LTN units. The majority of LTN cells, however, achieved maximal excitation at velocities between 0.8 and 12.8 degrees/s. The deepest inhibition was elicited over a range of velocities from 0.2 to 102.4 degrees/s, with two major peaks at 0.8 and 12.8 degrees/s. A similar range of velocity sensitivity was observed in DTN cells: maximal excitation was obtained for stimulus velocities from 1.6 to 102.4 degrees/s, with most DTN cells showing the greatest excitatory response between 6.4 and 12.8 degrees/s. A broad range of inhibitory velocity tuning was also observed in DTN units, with most cells exhibiting the deepest inhibitory modulation at 25.6 degrees/s. The majority of LTN and DTN units were driven most effectively through the eye contralateral to the recording site. Nonetheless, a large percentage of LTN (78%) and DTN (93%) cells could be driven to some extent through both eyes. Despite this conspicuous ipsilateral eye influence, no units were found in either the LTN or the DTN that were driven solely through the ipsilateral eye.(ABSTRACT TRUNCATED AT 400 WORDS)


1989 ◽  
Vol 61 (6) ◽  
pp. 1207-1220 ◽  
Author(s):  
M. J. Mustari ◽  
A. F. Fuchs

1. To determine the potential role of the primate accessory optic system (AOS) in optokinetic and smooth-pursuit eye movements, we recorded the activity of 110 single units in a subdivision of the AOS, the lateral terminal nucleus (LTN), in five alert rhesus macaques. All monkeys were trained to fixate a stationary target spot during visual testing and to track a small spot moving in a variety of visual environments. 2. LTN units formed a continuum of types ranging from purely visual to purely oculomotor. Visual units (50%) responded best for large-field (70 x 50 degrees), moving visual stimuli and had no response associated with smooth-pursuit eye movement; some responded during smooth pursuit in the dark, but the response disappeared if the target was briefly extinguished, indicating that their smooth-pursuit-related response reflected activation of a parafoveal receptive field. Eye movement and visual units (36%) responded both for large, moving visual stimuli and during smooth-pursuit eye movements made in the dark. Eye movement units (14%) discharged during smooth-pursuit or other eye movements but showed no evidence of visual sensitivity. 3. Essentially all (98%) LTN units were direction selective, responding preferentially during vertical background and/or smooth-pursuit movement. The vast majority (88%) preferred upward background and/or eye movement. During periodic movement of the large-field visual background while the animal fixated, their firing rates were modulated above and below rather high resting rates. Although LTN units typically responded best to movement of large-field stimuli, some also responded well to small moving stimuli (0.25 degrees diam). 4. LTN units could be separated into two populations according to their dependence on visual stimulus velocity. For periodic triangle wave stimuli, both types had velocity thresholds less than 3 degrees/s. As stimulus velocity increased above threshold, the activity of one type reached peak firing rates over a very narrow velocity range and remained nearly at peak firing for velocities from approximately 4-80 degrees/s. The firing rates of the other type exhibited velocity tuning in which the firing rate peaked at an average preferred velocity of 13 degrees/s and decreased for higher velocities. 5. A close examination of firing rates to sinusoidal background stimuli revealed that both unit types exhibited unusual behaviors at the extremes of stimulus velocity.(ABSTRACT TRUNCATED AT 400 WORDS)


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