scholarly journals The Accessory Optic System Contributes to the Spatio-Temporal Tuning of Motion-Sensitive Pretectal Neurons

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.

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.


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.


1995 ◽  
Vol 12 (1) ◽  
pp. 117-139 ◽  
Author(s):  
M.H. Rowe ◽  
L.A. Palmer

AbstractThe spatio-temporal receptive-field structure of 54 phasic W cells in cat retinas has been examined using the reverse-correlation method of Jones and Palmer (1987). Within this sample, 12 cells had on-center, 16 off-center, and 26 on-off receptive fields. Three of the on-center and seven of the on-off cells were directionally selective. Forty percent of the cells in this sample had local receptive fields consisting of two or more distinct subregions. However, no correlation was observed between the number of subregions in the local receptive field and other response properties such as center sign or direction selectivity. In all cases, individual subregions, including those in on-off cells, appear to be produced by a half-wave rectification of the input signal. For 76% of the cells, these local receptive fields were contained within large suppressive fields which could be seen to extend for at least 10 deg in all directions with no apparent spatial structure. The mechanism producing the suppressive field also appears to involve a rectification of the input signal, and has a relatively high spatial resolution. Furthermore, the suppressive field itself is only responsive to moving or flickering stimuli; large, stationary gratings have no effect on the output of the local receptive-field mechanism. Thus, the overall receptive-field organization of these cells is particularly well suited for detecting local motion. The remaining 24% of cells in the sample lacked suppressive fields, and consequently responded well to large moving stimuli, but these cells were otherwise similar in their receptive-field properties to cells with suppressive fields. The significance of these properties is discussed in the context of the projections of phasic W cells to the superior colliculus and accessory optic system.


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)


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)


2001 ◽  
Vol 86 (6) ◽  
pp. 2919-2930 ◽  
Author(s):  
Michael Ariel ◽  
Naoki Kogo

Neurons in turtle accessory optic system (basal optic nucleus, BON) were studied to compare excitatory and inhibitory visual inputs. Using a reduced in vitro brain stem preparation with the eyes attached, previous studies only showed a monosynaptic retinal input to the BON from direction-sensitive retinal ganglion cells that share a common preferred direction. Now using an intact brain stem preparation, not only did BON neurons display inhibitory postsynaptic potentials [IPSP(C)s] spontaneously, but IPSP(C)s were also evoked by visual pattern motion, they had their polarity reversed near the chloride equilibrium potential[Formula: see text] and they were blocked by the GABAA antagonist bicuculline. Because excitatory postsynaptic currents had reversal potentials >0 mV, BON cells were recorded using patch electrodes filled with QX-314 or Cs+ to measure the cell's direction tuning also at that higher reversal potential. For most of the BON neurons studied, their visual excitation and inhibition had a very similar preferred direction, indicating that both synaptic inputs were maximally active onto the same cell under the same stimulus conditions. These competing inputs may result from connections between the pretectum and accessory optic nuclei. Such synaptic interactions may serve a functional role in the visual processing necessary to create retinal slip signals for oculomotor control.


1991 ◽  
Vol 66 (2) ◽  
pp. 505-529 ◽  
Author(s):  
R. C. Reid ◽  
R. E. Soodak ◽  
R. M. Shapley

1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(ABSTRACT TRUNCATED AT 400 WORDS)


1998 ◽  
Vol 80 (6) ◽  
pp. 2882-2892 ◽  
Author(s):  
Christopher I. Moore ◽  
Sacha B. Nelson

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.


2005 ◽  
Vol 93 (4) ◽  
pp. 1959-1969 ◽  
Author(s):  
Michael Ariel ◽  
Naoki Kogo

The interaction of excitatory and inhibitory inputs to the accessory optic system was studied with whole cell recordings in the turtle basal optic nucleus. Previous studies have shown that visual patterns, drifting in the same preferred direction, evoke excitatory and inhibitory postsynaptic events simultaneously. Analysis of the reversal potentials for these events and their pharmacological profile suggest that they are mediated by AMPA and GABAA receptors, respectively. Here, neurons were recorded to study nonlinear interaction between excitatory and inhibitory responses evoked by electrical microstimulation of the retina and pretectum, respectively. The responses to coincident activation of excitatory and inhibitory inputs exhibited membrane shunting in that the excitatory response amplitude, adjusted for changes in driving force, was attenuated during the onset of the inhibitory response. This nonlinear interaction was seen in many but not all stimulus pairings. In some cases, attenuation was followed by an augmentation of the excitatory response. For comparison, the size of the excitatory response was evaluated during a hyperpolarizing current pulse that directly modulated voltage-sensitive channels of a slow rectifying Ih current. Injection of hyperpolarizing current did not cause the attenuation of the excitatory synaptic responses. We conclude that there is a nonlinear interaction between these excitatory and inhibitory synaptic currents that is not due to hyperpolarization itself, but probably is a result of their own synaptic conductance changes, i.e., shunting. Since these events are evoked by identical visual stimuli, this interaction may play a role in visual processing.


2002 ◽  
Vol 88 (2) ◽  
pp. 1026-1039 ◽  
Author(s):  
Steven F. Stasheff ◽  
Richard H. Masland

We recorded from on-off direction-selective ganglion cells (DS cells) in the rabbit retina to investigate in detail the inhibition that contributes to direction selectivity in these cells. Using paired stimuli moving sequentially across the cells' receptive fields in the preferred direction, we directly confirmed the prediction of Wyatt and Daw (1975) that a wave of inhibition accompanies any moving excitatory stimulus on its null side, at a fixed spatial offset. Varying the interstimulus distance, stimulus size, luminance, and speed yielded a spatiotemporal map of the strength of inhibition within this region. This “null” inhibition was maximal at an intermediate distance behind a moving stimulus: ½ to 1½ times the width of the receptive field. The strength of inhibition depended more on the distance behind the stimulus than on stimulus speed, and the inhibition often lasted 1–2 s. These spatial and temporal parameters appear to account for the known spatial frequency and velocity tuning of on-off DS cells to drifting contrast gratings. Stimuli that elicit distinct onand off responses to leading and trailing edges revealed that an excitatory response of either polarity could inhibit a subsequent response of either polarity. For example, an offresponse inhibited either an on or off response of a subsequent stimulus. This inhibition apparently is conferred by a neural element or network spanning the on andoff sublayers of the inner plexiform layer, such as a multistratified amacrine cell. Trials using a stationary flashing spot as a probe demonstrated that the total amount of inhibition conferred on the DS cell was equivalent for stimuli moving in either the null or preferred direction. Apparently the cell does not act as a classic “integrate and fire” neuron, summing all inputs at the soma. Rather, computation of stimulus direction likely involves interactions between excitatory and inhibitory inputs in local regions of the dendrites.


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