Spatiotemporal Tuning of Optic Flow Inputs to the Vestibulocerebellum in Pigeons: Differences Between Mossy and Climbing Fiber Pathways

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.

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.


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.


2002 ◽  
Vol 87 (3) ◽  
pp. 1554-1571 ◽  
Author(s):  
Kenji Yamamoto ◽  
Yasushi Kobayashi ◽  
Aya Takemura ◽  
Kenji Kawano ◽  
Mitsuo Kawato

To investigate how cerebellar synaptic plasticity guides the acquisition and adaptation of ocular following response (OFR), a large-scale network model was developed. The model includes the cerebral medial superior temporal area (MST), Purkinje cells (P cells) of the ventral paraflocculus, the accessory optic and climbing fiber systems, the brain stem oculomotor network, and the oculomotor plant. The model reconstructed temporal profiles of both firing patterns of MST neurons and P cells and eye movements. Model MST neurons ( n = 1,080) were set to be driven by retinal error and exhibited 12 preferred directions, 30 preferred velocities, and 3 firing waveforms. Correspondingly, each model P cell contained 1,080 excitatory synapses from granule cell axons (GCA) and 1,080 inhibitory synapses. P cells ( n = 40) were classified into four groups by their laterality (hemisphere) and by preferred directions of their climbing fiber inputs (CF) (contralateral or upward). The brain stem neural circuit and the oculomotor plant were modeled on the work of Yamamoto et al. The initial synaptic weights on the P cells were set randomly. At the beginning, P cell simple spikes were not well modulated by visual motion, and the eye was moved only slightly by the accessory optic system. The synaptic weights were updated according to integral-differential equation models of physiologically demonstrated synaptic plasticity: long-term depression and long-term potentiation for GCA synapses and rebound potentiation for inhibitory synapses. We assumed that maximum plasticity was induced when GCA inputs preceded CF inputs by 200 ms. After more than 10,000 presentations of ramp-step visual motion, the strengths of both the excitatory and inhibitory synapses were modified. Subsequently, the simple spike responses became well developed, and ordinary OFRs were acquired. The preferred directions of simple spikes became the opposite of those of CFs. Although the model MST neurons were set to possess a wide variety of firing characteristics, the model P cells acquired only downward or ipsilateral preferred directions, high preferred velocities and stereotypical firing waveforms. Therefore the drastic transition of the neural representation from the population codes in the MST to the firing-rate codes of simple spikes were learned at the GCA-P cell synapses and inhibitory cells-P cell synapses. Furthermore, the model successfully reproduced the gain- and directional-adaptation of OFR, which was demonstrated by manipulating the velocity and direction of visual motion, respectively. When we assumed that synaptic plasticity could only occur if CF inputs preceded GCA inputs, the ordinary OFR were acquired but neither the gain-adaptation nor the directional adaptation could be reproduced.


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.


1980 ◽  
Vol 43 (1) ◽  
pp. 46-59 ◽  
Author(s):  
F. Denoth ◽  
P. C. Magherini ◽  
O. Pompeiano ◽  
M. Stanojevic

1. The response of Purkinje (P) cells located in the vermal cortex of the cerebellar anterior lobe to sinusoidal rotation of the neck was investigated in precollicular decerebrate cats. The head of the animal was fixed in a sterotaxic frame while the spinous process of the second cervical vertebra was held by a clamp rigidly fixed to the tilting table. It was then possible to elicit a selective neck input by rotating the neck and the body simultaneously along the longitudinal axis of the animal while maintaining the head in horizontal position. 2. Among the 95 P-cells tested for neck stimulation, 35 units showed a mossy fiber (MF) or a climbing fiber (CF) response to sinusoidal rotation of the axis vertebra at the frequency of 0.026 Hz and at the peak amplitude of displacement of 5--10 degrees. The response consisted in a periodic modulation of the discharge frequency during sinusoidal rotation of the neck. Most of these units were excited during side-down rotation of the neck, but were inhibited during side-up rotation. 3. The threshold amplitude of neck rotation responsible for the MF-induced responses varied in different units from 1 to 3 degrees at the frequency of 0.026 Hz. The sensitivity of the units, expressed in percentage change of the average firing rate per degree of displacement, either did not change or very slightly decreased as a result of increasing amplitude of stimulation from 1--3 degrees to 10--15 degrees at the frequency of 0.026 Hz or by increasing frequency of neck rotation from 0.015 to 0.15 Hz at the amplitude of neck displacement of 5--10 degrees. 4. Changes in amplitude or frequency of stimulation at the parameters reported above did not greatly modify the phase of the unit responses relative to the side-down position of the neck. These findings indicate that the MF and CF responses of P-cells to sinusoidal rotation of the neck depended on changes in neck position and not on changes in velocity of neck rotation. 5. The observation that the majority of responding P-cells located in the vermal cortex of the cerebellar anterior lobe increased their firing rate during side-down rotation of the neck is discussed in relation to the results of stimulation and lesion experiments, indicating that postural changes can be elicited either during asymmetric stimulation of neck receptors or by unilateral interruption of the neck afferents.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Angela K Nietz ◽  
Jada H Vaden ◽  
Luke T Coddington ◽  
Linda Overstreet-Wadiche ◽  
Jacques I Wadiche

Golgi cells are the principal inhibitory neurons at the input stage of the cerebellum, providing feedforward and feedback inhibition through mossy fiber and parallel fiber synapses. In vivo studies have shown that Golgi cell activity is regulated by climbing fiber stimulation, yet there is little functional or anatomical evidence for synapses between climbing fibers and Golgi cells. Here, we show that glutamate released from climbing fibers activates ionotropic and metabotropic receptors on Golgi cells through spillover-mediated transmission. The interplay of excitatory and inhibitory conductances provides flexible control over Golgi cell spiking, allowing either excitation or a biphasic sequence of excitation and inhibition following single climbing fiber stimulation. Together with prior studies of spillover transmission to molecular layer interneurons, these results reveal that climbing fibers exert control over inhibition at both the input and output layers of the cerebellar cortex.


1997 ◽  
Vol 14 (5) ◽  
pp. 879-895 ◽  
Author(s):  
Helen Sherk ◽  
Kathleen Mulligan ◽  
Jong-Nam Kim

AbstractDuring locomotion, observers respond to objects in the environment that may represent obstacles to avoid or landmarks for navigation. Although much is known about how visual cortical neurons respond to stimulus objects moving against a blank background, nothing is known about their responses when objects are embedded in optic flow fields (the patterns of motion seen during locomotion). We recorded from cells in the lateral suprasylvian visual area (LS) of the cat, an area probably analogous to area MT. In our first experiments, optic flow simulations mimicked the view of a cat trotting across a plain covered with small balls; a black bar lying on the balls served as a target object. In subsequent experiments, optic flow simulations were composed of natural elements, with target objects representing bushes, rocks, and variants of these. Cells did not respond to the target bar in the presence of optic flow backgrounds, although they did respond to it in the absence of a background. However, 273/423 cells responded to at least one of the taller, naturalistic objects embedded in optic flow simulations. These responses might represent a form of image segmentation, in that cells detected objects against a complex background. Surprisingly, the responsiveness of cells to objects in optic flow fields was not correlated with preferred direction as measured with a moving bar or whole-field texture. Because the direction of object motion was determined solely by receptive-field location, it often differed considerably from a cell's preferred direction. About a quarter of the cells responded well to objects in optic flow movies but more weakly or not at all to bars moving in the same direction as the object, suggesting that the optic flow background modified or suppressed direction selectivity.


2019 ◽  
Author(s):  
Florian A. Dehmelt ◽  
Rebecca Meier ◽  
Julian Hinz ◽  
Takeshi Yoshimatsu ◽  
Clara A. Simacek ◽  
...  

AbstractMany animals have large visual fields, and sensory circuits may sample those regions of visual space most relevant to behaviours such as gaze stabilisation and hunting. Despite this, relatively small displays are often used in vision neuroscience. To sample stimulus locations across most of the visual field, we built a spherical stimulus arena with 14,848 independently controllable LEDs, measured the optokinetic response gain of immobilised zebrafish larvae, and related behaviour to previously published retinal photoreceptor densities. We measured tuning to steradian stimulus size and spatial frequency, and show it to be independent of visual field position. However, zebrafish react most strongly and consistently to lateral, nearly equatorial stimuli, consistent with previously reported higher spatial densities in the central retina of red, green and blue photoreceptors. Upside-down experiments suggest further extra-retinal processing. Our results demonstrate that motion vision circuits in zebrafish are anisotropic, and preferentially monitor areas with putative behavioural relevance.Author summaryThe visual system of larval zebrafish mirrors many features present in the visual system of other vertebrates, including its ability to mediate optomotor and optokinetic behaviour. Although the presence of such behaviours and some of the underlying neural correlates have been firmly established, previous experiments did not consider the large visual field of zebrafish, which covers more than 160° for each eye. Given that different parts of the visual field likely carry unequal amount of behaviourally relevant information for the animal, this raises the question whether optic flow is integrated across the entire visual field or just parts of it, and how this shapes behaviour such as the optokinetic response. We constructed a spherical LED arena to present visual stimuli almost anywhere across their visual field, while tracking horizontal eye movements. By displaying moving gratings on this LED arena, we demonstrate that the optokinetic response, one of the most prominent visually induced behaviours of zebrafish, indeed strongly depends on stimulus location and stimulus size, as well as on other parameters such as the spatial and temporal frequency of the gratings. This location dependence is consistent with areas of high retinal photoreceptor densities, though evidence suggests further extraretinal processing.


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