Shunting Inhibition in Accessory Optic System Neurons

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.

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Direction Tuning of Inhibitory Inputs to the Turtle Accessory Optic System

Journal of Neurophysiology ◽

10.1152/jn.2001.86.6.2919 ◽

2001 ◽

Vol 86 (6) ◽

pp. 2919-2930 ◽

Cited By ~ 9

Author(s):

Michael Ariel ◽

Naoki Kogo

Keyword(s):

Brain Stem ◽

Visual Processing ◽

Reversal Potential ◽

Oculomotor Control ◽

Equilibrium Potential ◽

Optic System ◽

Accessory Optic System ◽

Preferred Direction ◽

Direction Tuning

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.

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Morphology of the turtle accessory optic system

Visual Neuroscience ◽

10.1017/s0952523803206064 ◽

2003 ◽

Vol 20 (6) ◽

pp. 639-649 ◽

Cited By ~ 3

Author(s):

JOHN MARTIN ◽

NAOKI KOGO ◽

TIAN XING FAN ◽

MICHAEL ARIEL

Keyword(s):

Visual Processing ◽

Ganglion Cells ◽

Computer Software ◽

Dorsal Side ◽

Visual Responses ◽

Optic System ◽

Neural Signals ◽

Accessory Optic System ◽

Full Field

Neural signals of the moving visual world are detected by a subclass of retinal ganglion cells that project to the accessory optic system in the vertebrate brainstem. We studied the dendritic morphologies and direction tuning of these brainstem neurons in turtle (Pseudemys scripta elegans) to understand their role in visual processing. Full-field checkerboard patterns were drifted on the contralateral retina while whole-cell recordings were made in the basal optic nucleus in an intact brainstem preparation in vitro. Neurobiotin diffused into the neurons during the recording and was subsequently localized in brain sections. Neuronal morphologies were traced using appropriate computer software to analyze their position in the brainstem. Most labeled neurons were fusiform in shape and had numerous varicosities along their processes. The majority of dendritic trees spread out in a transverse plane perpendicular to the rostrocaudal axis of the nucleus. Neurons near the brainstem surface were often oriented tangential to that surface, whereas more cells at the dorsal side of the nucleus were oriented radial to the brainstem surface. Further analysis of Nissl-stained neurons revealed the largest neurons are located in the rostral and medial portions of the nucleus although neurons are most densely packed in the middle of the nucleus. The preferred directions of the visual responses of the neurons in this sample did not correlate with their morphology and position in the nucleus. Therefore, the morphology of the cells in the turtle accessory optic system appears dependent on its position within the nucleus while its visual responses may depend on the synaptic inputs that contact each cell.

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

Journal of Neurophysiology ◽

10.1152/jn.00653.2002 ◽

2003 ◽

Vol 90 (2) ◽

pp. 1140-1151 ◽

Cited By ~ 17

Author(s):

Nathan A. Crowder ◽

Hugo Lehmann ◽

Marise B. Parent ◽

Douglas R.W. Wylie

Keyword(s):

Receptive Fields ◽

Sine Wave ◽

Excitatory Input ◽

Direction Selectivity ◽

Oculomotor Control ◽

Optic System ◽

Accessory Optic System ◽

Preferred Direction ◽

Before And After ◽

Spatio Temporal

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.

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Connectivity of the turtle accessory optic system

Brain Research ◽

10.1016/s0006-8993(03)03371-7 ◽

2003 ◽

Vol 989 (1) ◽

pp. 76-90 ◽

Cited By ~ 5

Author(s):

Amy E Weber ◽

John Martin ◽

Michael Ariel

Keyword(s):

Optic System ◽

Accessory Optic System

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Evidence for glycine, GABAA, and GABAB receptors on rabbit OFF-alpha ganglion cells

Visual Neuroscience ◽

10.1017/s0952523803203072 ◽

2003 ◽

Vol 20 (3) ◽

pp. 285-296 ◽

Cited By ~ 12

Author(s):

THOMAS C. ROTOLO ◽

RAMON F. DACHEUX

Keyword(s):

Ganglion Cells ◽

Gabab Receptors ◽

Direct Inhibition ◽

Light Responses ◽

Retinal Surface ◽

Excitatory Response ◽

Sulforhodamine B ◽

Intact Rabbit ◽

Specific Receptors ◽

Whole Cell Recordings

Inhibitory synaptic transmission via GABA and glycine receptors plays a crucial role in shaping the excitatory response of neurons in the retina. Whole-cell recordings were obtained from ganglion cells in the intact rabbit eyecup preparation to correlate GABA- and glycine-activated currents with the presence of their specific receptors on morphologically identified α ganglion cells. Alpha ganglion cells were chosen based upon their large somata when viewing the retinal surface, and responses to light and dark spots were used to identify OFF-alpha ganglion cells. Light responses were abolished by superfusion of Ringer's containing cobalt to synaptically isolate the cell by blocking all Ca2+-mediated transmitter release. Pressure pulses of GABA and glycine were delivered to an area that encompassed the dendritic field while receptor antagonists were applied through superfusion to characterize the direct inhibition onto the ganglion cell. Physiological results indicated that OFF-α cells did not have any GABAC receptor-activated currents, but did express currents mediated by ionotropic GABAA receptors and metabotropic GABAB receptors that were blocked by their specific antagonists bicuculline and CGP55845, respectively. The amplitudes of strychnine-sensitive glycine-activated currents were always larger than the currents elicited by GABA. Confocal optical sections of physiologically identified, sulforhodamine B-stained cells displayed the localization of glycine and GABAA receptor subunit labeling dispersed over the stained dendrites.

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OKN-related neurons in the rat nucleus of the optic tract and dorsal terminal nucleus of the accessory optic system receive a direct cortical input

The Journal of Comparative Neurology ◽

10.1002/cne.903300202 ◽

1993 ◽

Vol 330 (2) ◽

pp. 147-157 ◽

Cited By ~ 23

Author(s):

M. Schmidt ◽

H.-Y. Zhang ◽

K.-P. Hoffmann

Keyword(s):

Optic Tract ◽

Optic System ◽

Accessory Optic System ◽

Cortical Input

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Monaural inhibition in cat auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.1995.73.5.1876 ◽

1995 ◽

Vol 73 (5) ◽

pp. 1876-1891 ◽

Cited By ~ 187

Author(s):

M. B. Calford ◽

M. N. Semple

Keyword(s):

Auditory Cortex ◽

Lateral Inhibition ◽

Cortical Neurons ◽

Frequency Tuning ◽

Inhibitory Response ◽

Forward Masking ◽

Excitatory Response ◽

Rate Level ◽

Wide Range ◽

Response Area

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)

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Evidence for a supplementary eye field

Journal of Neurophysiology ◽

10.1152/jn.1987.57.1.179 ◽

1987 ◽

Vol 57 (1) ◽

pp. 179-200 ◽

Cited By ~ 369

Author(s):

J. Schlag ◽

M. Schlag-Rey

Keyword(s):

Unit Activity ◽

Cortical Neurons ◽

Cortical Area ◽

Head Movements ◽

Frontal Eye Field ◽

Unit Recording ◽

Electrical Microstimulation ◽

Preferred Direction ◽

Supplementary Eye Field ◽

Eye Field

Electrical microstimulation and unit recording were performed in dorsomedial frontal cortex of four alert monkeys to identify an oculomotor area whose existence had been postulated rostral to the supplementary motor area. Contraversive saccades were evoked from 129 sites by stimulation. Threshold currents were lower than 20 microA in half the tests. Response latencies were usually longer than 50 ms (minimum: 30 ms). Eye movements were occasionally accompanied by blinks, ear, or neck movements. The cortical area yielding these movements was at the superior edge of the frontal lobe just rostral to the region from which limb movements could be elicited. Depending on the site of stimulation, saccades varied between two extremes: from having rather uniform direction and size, to converging toward a goal defined in space. The transition between these extremes was gradual with no evidence that these two types were fundamentally different. From surface to depth of cortex, direction and amplitude of evoked saccades were similar or changed progressively. No clear systematization was found depending on location along rostrocaudal or mediolateral axes of the cortex. The dorsomedial oculomotor area mapped was approximately 7 mm long and 6 mm wide. Combined eye and head movements were elicited from one of ten sites stimulated when the head was unrestrained. In the other nine cases, saccades were not accompanied by head rotation, even when higher currents or longer stimulus trains were applied. Presaccadic unit activity was recorded from 62 cells. Each of these cells had a preferred direction that corresponded to the direction of the movement evoked by local microstimulation. Presaccadic activity occurred with self-initiated as well as visually triggered saccades. It often led self-initiated saccades by more than 300 ms. Recordings made with the head free showed that the firing could not be interpreted as due to attempted head movements. Many dorsomedial cortical neurons responded to photic stimuli, either phasically or tonically. Sustained responses (activation or inhibition) were observed during target fixation. Twenty-one presaccadic units showed tonic changes of activity with fixation. Justification is given for considering the cortical area studied as a supplementary eye field. It shares many common properties with the arcuate frontal eye field. Differences noted in this study include: longer latency of response to electrical stimulation, possibility to evoke saccades converging apparently toward a goal, and long-lead unit activity with spontaneous saccades.

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