The computation of directional selectivity in the Drosophila OFF motion pathway

In flies, the direction of moving ON and OFF features is computed separately. T4 (ON) and T5 (OFF) are the first neurons in their respective pathways to extract a directionally selective response from their non-selective inputs. Our recent study of T4 found that the integration of offset depolarizing and hyperpolarizing inputs is critical for the generation of directional selectivity. However, T5s lack small-field inhibitory inputs, suggesting they may use a different mechanism. Here we used whole-cell recordings of T5 neurons and found a similar receptive field structure: fast depolarization and persistent, spatially offset hyperpolarization. By assaying pairwise interactions of local stimulation across the receptive field, we found no amplifying responses, only suppressive responses to the non-preferred motion direction. We then evaluated passive, biophysical models and found that a model using direct inhibition, but not the removal of excitation, can accurately predict T5 responses to a range of moving stimuli.

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The computation of directional selectivity in the Drosophila OFF motion pathway

10.1101/721902 ◽

2019 ◽

Author(s):

Eyal Gruntman ◽

Sandro Romani ◽

Michael B. Reiser

Keyword(s):

Receptive Field ◽

Visual Motion ◽

Biophysical Model ◽

Functional Studies ◽

Moving Stimuli ◽

Local Inhibition ◽

Pairwise Interactions ◽

Fast Excitation ◽

Whole Cell Recordings ◽

Local Stimulation

AbstractThe direction of visual motion in Drosophila is computed by separate pathways for moving ON and OFF features. The 4th order neurons T4 (ON) and T5 (OFF) are the first neurons in their respective pathways to extract a directionally selective response from their non-selective inputs. Recent functional studies have found a major role for local inhibition in the generation of directionally selective responses. However, T5 lacks small-field inhibitory inputs. Here we use whole-cell recordings of T5 neurons and find an asymmetric receptive field structure, with fast excitation and persistent, spatially trailing inhibition. We assayed pairwise interactions of local stimulation across the receptive field, and find no active amplification, only passive suppression. We constructed a biophysical model of T5 based on the classic Receptive Field. This model, which lacks active conductances and was tuned only to match non-moving stimuli, accurately predicts responses to complex moving stimuli.

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Computation of motion direction by quail retinal ganglion cells that have a nonconcentric receptive field

Visual Neuroscience ◽

10.1017/s0952523800172086 ◽

2000 ◽

Vol 17 (2) ◽

pp. 263-271 ◽

Cited By ~ 8

Author(s):

HIROYUKI UCHIYAMA ◽

TAKAHIDE KANAYA ◽

SHOICHI SONOHATA

Keyword(s):

Receptive Field ◽

Retinal Ganglion Cells ◽

Japanese Quail ◽

Ganglion Cells ◽

Receptive Fields ◽

Object Motion ◽

Directional Selectivity ◽

Retinal Ganglion ◽

Motion Direction ◽

Neuronal Mechanisms

One type of retinal ganglion cells prefers object motion in a particular direction. Neuronal mechanisms for the computation of motion direction are still unknown. We quantitatively mapped excitatory and inhibitory regions of receptive fields for directionally selective retinal ganglion cells in the Japanese quail, and found that the inhibitory regions are displaced about 1–3 deg toward the side where the null sweep starts, relative to the excitatory regions. Directional selectivity thus results from delayed transient suppression exerted by the nonconcentrically arranged inhibitory regions, and not by local directional inhibition as hypothesized by Barlow and Levick (1965).

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Functional and physiological models as revealed by visual receptive field structure

Neuroscience Research ◽

10.1016/s0168-0102(00)80924-4 ◽

2000 ◽

Vol 38 ◽

pp. S12

Author(s):

I Ohzawa

Keyword(s):

Receptive Field ◽

Field Structure ◽

Physiological Models ◽

Visual Receptive Field

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Faculty Opinions recommendation of Natural stimulus statistics alter the receptive field structure of v1 neurons.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1020838.239489 ◽

2004 ◽

Author(s):

Kathleen Cullen

Keyword(s):

Receptive Field ◽

Field Structure ◽

Natural Stimulus ◽

V1 Neurons

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Faculty Opinions recommendation of Receptive field structure varies with layer in the primary visual cortex.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1024414.287911 ◽

2005 ◽

Author(s):

Matteo Carandini

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Primary Visual Cortex ◽

Field Structure

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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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Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons

Experimental Brain Research ◽

10.1007/s002210100849 ◽

2001 ◽

Vol 141 (1) ◽

pp. 88-100 ◽

Cited By ~ 45

Author(s):

Asif Ghazanfar ◽

David Krupa ◽

Miguel Nicolelis

Keyword(s):

Receptive Field ◽

Nonlinear Response ◽

Field Structure ◽

Thalamic Neurons ◽

Response Properties ◽

Cortical Feedback

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DEVELOPMENT OF FEEDFORWARD RECEPTIVE FIELD STRUCTURE OF A SIMPLE CELL AND ITS CONTRIBUTION TO THE ORIENTATION SELECTIVITY: A MODELING STUDY

International Journal of Neural Systems ◽

10.1142/s0129065705000104 ◽

2005 ◽

Vol 15 (01n02) ◽

pp. 55-70 ◽

Cited By ~ 1

Author(s):

AKHIL R GARG ◽

KLAUS OBERMAYER ◽

BASABI BHAUMIK

Keyword(s):

Receptive Field ◽

Field Structure ◽

Orientation Selectivity ◽

Simple Cell ◽

Homogeneous State ◽

Synaptic Efficacy ◽

Synaptic Interactions ◽

Experimental Findings ◽

Modeling Study

Recent experimental studies of hetero-synaptic interactions in various systems have shown the role of signaling in the plasticity, challenging the conventional understanding of Hebb's rule. It has also been found that activity plays a major role in plasticity, with neurotrophins acting as molecular signals translating activity into structural changes. Furthermore, role of synaptic efficacy in biasing the outcome of competition has also been revealed recently. Motivated by these experimental findings we present a model for the development of simple cell receptive field structure based on the competitive hetero-synaptic interactions for neurotrophins combined with cooperative hetero-synaptic interactions in the spatial domain. We find that with proper balance in competition and cooperation, the inputs from two populations (ON/OFF) of LGN cells segregate starting from the homogeneous state. We obtain segregated ON and OFF regions in simple cell receptive field. Our modeling study supports the experimental findings, suggesting the role of synaptic efficacy and the role of spatial signaling. We find that using this model we obtain simple cell RF, even for positively correlated activity of ON/OFF cells. We also compare different mechanism of finding the response of cortical cell and study their possible role in the sharpening of orientation selectivity. We find that degree of selectivity improvement in individual cells varies from case to case depending upon the structure of RF field and type of sharpening mechanism.

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