scholarly journals The computation of directional selectivity in the Drosophila OFF motion pathway

2019 ◽  
Author(s):  
Eyal Gruntman ◽  
Sandro Romani ◽  
Michael B. Reiser

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.

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Eyal Gruntman ◽  
Sandro Romani ◽  
Michael B Reiser

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.


2015 ◽  
Vol 112 (15) ◽  
pp. E1956-E1965 ◽  
Author(s):  
Andreas A. Kardamakis ◽  
Kazuya Saitoh ◽  
Sten Grillner

The optic tectum (called superior colliculus in mammals) is critical for eye–head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex—yet phylogenetically conserved—sensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gaze-controlling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution.


1999 ◽  
Vol 82 (5) ◽  
pp. 2462-2475 ◽  
Author(s):  
Satoshi Eifuku ◽  
Robert H. Wurtz

Many neurons in the lateral-ventral region of the medial superior temporal area (MSTl) have a clear center surround separation in their receptive fields. Either moving or stationary stimuli in the surround modulates the response to moving stimuli in the center, and this modulation could facilitate the perceptual segmentation of a moving object from its background. Another mechanism that could facilitate such segmentation would be sensitivity to binocular disparity in the center and surround regions of the receptive fields of these neurons. We therefore investigated the sensitivity of these MSTl neurons to disparity ranging from three degrees crossed disparity (near) to three degrees uncrossed disparity (far) applied to both the center and the surround regions. Many neurons showed clear disparity sensitivity to stimulus motion in the center of the receptive field. About [Formula: see text] of 104 neurons had a clear peak in their response, whereas another [Formula: see text] had broader tuning. Monocular stimulation abolished the tuning. The prevalence of cells broadly tuned to near and far disparity and the reversal of preferred directions at different disparities observed in MSTd were not found in MSTl. A stationary surround at zero disparity simply modulated up or down the response to moving stimuli at different disparities in the receptive field (RF) center but did not alter the disparity tuning curve. When the RF center motion was held at zero disparity and the disparity of the stationary surround was varied, some surround disparities produced greater modulation of MSTl neuron response than did others. Some neurons with different disparity preferences in center and surround responded best to the relative disparity differences between center and surround, whereas others were related to the absolute difference between center and surround. The combination of modulatory surrounds and the sensitivity to relative difference between center and surround disparity make these MSTl neurons particularly well suited for the segmentation of a moving object from the background.


2006 ◽  
Vol 95 (6) ◽  
pp. 3712-3726 ◽  
Author(s):  
Frédéric V. Barthélemy ◽  
Ivo Vanzetta ◽  
Guillaume S. Masson

Visual neurons integrate information over a finite part of the visual field with high selectivity. This classical receptive field is modulated by peripheral inputs that play a role in both neuronal response normalization and contextual modulations. However, the consequences of these properties for visuomotor transformations are yet incompletely understood. To explore those, we recorded short-latency ocular following responses in humans to large center-only and center-surround stimuli. We found that eye movements are triggered by a mechanism that integrates motion over a restricted portion of the visual field, the size of which depends on stimulus contrast and increases as a function of time after response onset. We also found evidence for a strong nonisodirectional center-surround organization, responsible for normalizing the central, driving input so that motor responses are set to their most linear contrast dynamics. Such response normalization is delayed about 20 ms relative to tracking onset, gradually builds up over time, and is partly tuned for surround orientation/direction. These results outline the spatiotemporal organization of a behavioral receptive field, which might reflect a linear integration among subpopulations of cortical visual motion detectors.


2008 ◽  
Vol 100 (2) ◽  
pp. 646-656 ◽  
Author(s):  
Ben Scholl ◽  
Michael Wehr

Sensory deafferentation results in rapid shifts in the receptive fields of cortical neurons, but the synaptic mechanisms underlying these changes remain unknown. The rapidity of these shifts has led to the suggestion that subthreshold inputs may be unmasked by a selective loss of inhibition. To study this, we used in vivo whole cell recordings to directly measure tone-evoked excitatory and inhibitory synaptic inputs in auditory cortical neurons before and after acoustic trauma. Here we report that acute acoustic trauma disrupted the balance of excitation and inhibition by selectively increasing and reducing the strength of inhibition at different positions within the receptive field. Inhibition was abolished for frequencies far below the trauma-tone frequency but was markedly enhanced near the edges of the region of elevated peripheral threshold. These changes occurred for relatively high-level tones. These changes in inhibition led to an expansion of receptive fields but not by a simple unmasking process. Rather, membrane potential responses were delayed and prolonged throughout the receptive field by distinct interactions between synaptic excitation and inhibition. Far below the trauma-tone frequency, decreased inhibition combined with prolonged excitation led to increased responses. Near the edges of the region of elevated peripheral threshold, increased inhibition served to delay rather than abolish responses, which were driven by prolonged excitation. These results show that the rapid receptive field shifts caused by acoustic trauma are caused by distinct mechanisms at different positions within the receptive field, which depend on differential disruption of excitation and inhibition.


2005 ◽  
Vol 94 (2) ◽  
pp. 1104-1114 ◽  
Author(s):  
Katsuyuki Kaneda ◽  
Hitoshi Kita

The globus pallidus (GP) contains abundant GABAergic synapses and GABAB receptors. To investigate whether synaptically released GABA can activate pre- and postsynaptic GABAB receptors in the GP, physiological recordings were performed using rat brain slice preparations. Cell-attached recordings from GABAA antagonist-treated preparations revealed that repetitive local stimulation induced a GABAB antagonist-sensitive pause in spontaneous firings of GP neurons. Whole cell recordings revealed that the repetitive stimulation evoked fast excitatory postsynaptic potentials followed by a slow inhibitory postsynaptic potential (IPSP) in GP neurons. The slow IPSP was insensitive to a GABAA receptor antagonist, increased in amplitude with the application of ionotropic glutamate receptor antagonists, and was suppressed by the GABAB antagonist CGP55845 . The reversal potential of the slow IPSP was close to the potassium equilibrium potential. These results suggest that synaptically released GABA activated postsynaptic GABAB receptors and induced the pause and the slow IPSP. On the other hand, in the neurons that were treated to block postsynaptic GABAB responses, CGP55845 increased the amplitudes of repetitive local stimulation-induced GABAA-mediated inhibitory postsynaptic currents (IPSCs) but not the ionotropic glutamate-mediated excitatory postsynaptic currents. Moreover, the GABAB receptor specific agonist baclofen reduced the frequency of miniature IPSCs without altering their amplitude distributions. These results suggest that synaptically released GABA also activated presynaptic GABAB autoreceptors, resulting in decreased GABA release in the GP. Together, we infer that both pre- and postsynaptic GABAB receptors may play crucial roles in the control of GP neuronal activity.


2017 ◽  
Vol 5 (5) ◽  
pp. 827-842 ◽  
Author(s):  
Kimberly B. Schauder ◽  
Woon Ju Park ◽  
Duje Tadin ◽  
Loisa Bennetto

Atypical visual motion perception has been widely observed in individuals with autism spectrum disorder (ASD). The pattern of results, however, has been inconsistent. Emerging mechanistic hypotheses seek to explain these variable patterns of atypical motion sensitivity, each uniquely predicting specific patterns of performance across varying stimulus conditions. Here, we investigated the integrity of two such fundamental mechanisms—response gain control and receptive field size. A total of 20 children and adolescents with ASD and 20 typically developing (TD) age- and IQ-matched controls performed a motion discrimination task. To adequately model group differences in both mechanisms of interest, we tested a range of 23 stimulus conditions varying in size and contrast. Results revealed a motion perception impairment in ASD that was specific to the smallest sized stimuli (1°), irrespective of stimulus contrast. Model analyses provided evidence for larger receptive field size in ASD as the mechanism that explains this size-specific reduction of motion sensitivity.


1998 ◽  
Vol 80 (1) ◽  
pp. 282-296 ◽  
Author(s):  
Satoshi Eifuku ◽  
Robert H. Wurtz

Eifuku, Satoshi and Robert H. Wurtz. Response to motion in extrastriate area MSTl: center-surround interactions. J. Neurophysiol. 80: 282–296, 1998. The medial superior temporal area of the macaque monkey extrastriate visual cortex can be divided into a dorsal medial (MSTd) and a lateral ventral (MSTl) region. The functions of the two regions may not be identical: MSTd may process optic flow information that results from the movement of the observer, whereas MSTl may be related more closely to processing visual motion related specifically to the motion of objects. If MSTl were related to such object motion, one would expect to see mechanisms for the segregation of objects from their surround. We investigated one of these mechanisms in MSTl neurons: the effect of stimuli falling in the region surrounding the receptive field center on the response to stimuli falling in the field center. We found the effects of the surround stimulation to be modulatory with little response to the surround stimulus itself but a clear effect on the response to the stimulus falling on the receptive field center. The response to motion in the center in the direction preferred for the neuron usually increased when the surround motion was in the opposite direction to that in the center and decreased when surround motion was in the same direction as that in the center. Fifty-seven percent of the neurons showed a ratio of response for center motion with a surround moving in the opposite direction to that in the center for center motion alone that was >1. The response to motion in the center also increased when the surround stimulus was stationary, and this increase was sometimes larger than that with a moving surround. Nearly 70% of the neurons showed a ratio of response to center motion with a stationary surround to center motion alone that was >1. This is in contrast to the minimal effect of stationary surrounds in middle temporal area neurons. When the stimulus presentation was reversed so that the stimulus in the center was stationary and the surround moved, some MSTl neurons responded when the direction of motion in the surround was in the direction opposite to the preferred direction of motion in the center of the receptive field. Stimulation of the surround thus had a profound effect on the response of MSTl neurons, and this pronounced effect of the surround is consistent with a role in the segmentation of objects using motion.


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