Mechanisms underlying direction selectivity of neurons in the primary visual cortex of the macaque

1995 ◽  
Vol 74 (4) ◽  
pp. 1382-1394 ◽  
Author(s):  
H. Sato ◽  
N. Katsuyama ◽  
H. Tamura ◽  
Y. Hata ◽  
T. Tsumoto
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Threshold Level ◽  
Intracortical Inhibition ◽  
Direction Selectivity ◽  
Gamma Aminobutyric Acid ◽  
Visual Responses ◽  
Preferred Direction ◽  
Control Response ◽  
Layer Vi

1. We studied the effects of blocking intracortical inhibition by microiontophoretic administration of bicuculline methiodide (BMI), a selective antagonist for gamma-aminobutyric acid-A receptors, on direction sensitivity of 103 neurons in the primary visual cortex (VI) of anesthetized and paralyzed monkeys. 2. The direction selectivity index (DSI) of each cell was calculated for the control response and response during the BMI administration at the optimal stimulus orientation to assess the directionality of an individual cell. 3. The averaged direction tuning of visual responses of cells was sharp in layers IVa and IVb, moderate in both interblob and blob regions of layer II/III and layers V and VI, and poor in layers IVc alpha and IVc beta. 4. Iontophoretic administration of BMI uncovered or facilitated responses to stimuli moving in the nonpreferred direction, and reduced DSIs of cells to a varying extent in all the layers except layer VI. Responses to stimuli moving in the preferred direction were also facilitated so that a slight bias of response toward the originally preferred direction remained during BMI administration in most cells. 5. Most of the cells in layers II/III (both blobs and interblobs) and IVb that receive inputs from layers IVc alpha and IVc beta showed a clear reduction of direction selectivity during BMI administration. This result suggests that intracortical inhibition plays an important role in the elaboration of direction selectivity at the second stage of information processing in VI. 6. The direction selectivity of cells in layer VI was most resistant to the effects of BMI, suggesting that it is dependent on excitatory inputs that are already direction selective, even though the sample size of this layer was small. 7. In direction-selective cells outside layer VI, responses to a stimulus moving in the preferred direction were enhanced in a way that was linearly related with those in the nonpreferred direction as the BMI dose was increased. This suggests that various amounts of inhibition interact linearly with directionally biased excitatory inputs to raise the firing threshold to various levels so as to produce various degrees of directionality. 8. These results suggest that, in most of the directionally sensitive cells except for those in layer VI, there are excitatory inputs which are bidirectional but slightly biased to one direction, and that the intracortical inhibition raises a threshold level of responses to excitatory inputs so that the response become direction selective.

scholarly journals Pure tones modulate the representation of orientation and direction in the primary visual cortex

2019 ◽  
Vol 121 (6) ◽  
pp. 2202-2214 ◽  
Author(s):  
John P. McClure ◽  
Pierre-Olivier Polack
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulus ◽  
Visual Stimuli ◽  
Direction Selectivity ◽  
Multimodal Integration ◽  
Visual Responses ◽  
V1 Neurons ◽  
Pure Tones ◽  
The Impact

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. Whereas multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. In the present study, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multimodal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue’s orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone. NEW & NOTEWORTHY The primary visual cortex (V1) receives direct inputs from the primary auditory cortex. Yet, the impact of sounds on visual processing in V1 remains controverted. We show that the modulation by pure tones of V1 visual responses depends on the orientation selectivity, direction selectivity, and response amplitudes of V1 neurons. Hence, audiovisual stimuli recruit a population of V1 neurons better tuned to the orientation and direction of the visual stimulus than unimodal visual stimuli.

scholarly journals A theory of direction selectivity for macaque primary visual cortex

2021 ◽  
Vol 118 (32) ◽  
pp. e2105062118
Author(s):  
Logan Chariker ◽  
Robert Shapley ◽  
Michael Hawken ◽  
Lai-Sang Young
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Cortical Cell ◽  
Direction Selectivity ◽  
Complete Analysis ◽  
Visual Response ◽  
Response Dynamics ◽  
Preferred Direction

This paper offers a theory for the origin of direction selectivity (DS) in the macaque primary visual cortex, V1. DS is essential for the perception of motion and control of pursuit eye movements. In the macaque visual pathway, neurons with DS first appear in V1, in the Simple cell population of the Magnocellular input layer 4Cα. The lateral geniculate nucleus (LGN) cells that project to these cortical neurons, however, are not direction selective. We hypothesize that DS is initiated in feed-forward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of 1) different visual response dynamics of ON and OFF LGN cells and 2) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that, together with item 2, produce distinct response time courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Cα in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broadband in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.

scholarly journals Mechanisms of Direction Selectivity in Cat Primary Visual Cortex as Revealed by Visual Adaptation

2010 ◽  
Vol 104 (5) ◽  
pp. 2615-2623 ◽  
Author(s):  
Nicholas J. Priebe ◽  
Ilan Lampl ◽  
David Ferster
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Direction Selectivity ◽  
Dependent Manner ◽  
Visual Responses ◽  
Null Direction ◽  
Simple Cells ◽  
Complex Cells

In contrast to neurons of the lateral geniculate nucleus (LGN), neurons in the primary visual cortex (V1) are selective for the direction of visual motion. Cortical direction selectivity could emerge from the spatiotemporal configuration of inputs from thalamic cells, from intracortical inhibitory interactions, or from a combination of thalamic and intracortical interactions. To distinguish between these possibilities, we studied the effect of adaptation (prolonged visual stimulation) on the direction selectivity of intracellularly recorded cortical neurons. It is known that adaptation selectively reduces the responses of cortical neurons, while largely sparing the afferent LGN input. Adaptation can therefore be used as a tool to dissect the relative contribution of afferent and intracortical interactions to the generation of direction selectivity. In both simple and complex cells, adaptation caused a hyperpolarization of the resting membrane potential (−2.5 mV, simple cells, −0.95 mV complex cells). In simple cells, adaptation in either direction only slightly reduced the visually evoked depolarization; this reduction was similar for preferred and null directions. In complex cells, adaptation strongly reduced visual responses in a direction-dependent manner: the reduction was largest when the stimulus direction matched that of the adapting motion. As a result, adaptation caused changes in the direction selectivity of complex cells: direction selectivity was reduced after preferred direction adaptation and increased after null direction adaptation. Because adaptation in the null direction enhanced direction selectivity rather than reduced it, it seems unlikely that inhibition from the null direction is the primary mechanism for creating direction selectivity.

scholarly journals Morphological and Physiological Characterization of Layer VI Corticofugal Neurons of Mouse Primary Visual Cortex

2003 ◽  
Vol 89 (5) ◽  
pp. 2854-2867 ◽  
Author(s):  
Joshua C. Brumberg ◽  
Farid Hamzei-Sichani ◽  
Rafael Yuste
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Action Potentials ◽  
Three Dimensional ◽  
Cell Types ◽  
Dorsal Lateral Geniculate Nucleus ◽  
Morphological Properties ◽  
Feedback Connection ◽  
Physiological Characterization ◽  
Layer Vi

Layer VI is the origin of the massive feedback connection from the cortex to the thalamus, yet its complement of cell types and their connections is poorly understood. The physiological and morphological properties of corticofugal neurons of layer VI of mouse primary visual cortex were investigated in slices loaded with the Ca2+indicator fura-2AM. To identify corticofugal neurons, electrical stimulation of the white matter (WM) was done in conjunction with calcium imaging to detect neurons that responded with changes in intracellular Ca2+ concentrations in response to the stimulation. Subsequent whole cell recordings confirmed that they discharged antidromic action potentials after WM stimulation. Antidromically activated neurons were more excitable and had different spiking properties than neighboring nonantidromic neurons, although both groups had similar input resistances. Furthermore, antidromic neurons possessed narrower action potentials and smaller afterhyperpolarizations. Additionally, three-dimensional reconstructions indicated that antidromically activated neurons had a distinct morphology with longer apical dendrites and fewer nonprimary dendrites than nonantidromic cells. To identify the antidromic neurons, rhodamine microspheres were injected into the dorsal lateral geniculate nucleus of the thalamus and allowed to retrogradely transport back to the somata of the layer VI cortico-geniculate neurons. Physiological and anatomical analysis indicated that most antidromic neurons were likely to be cortico-geniculate neurons. Our results show that cortico-thalamic neurons represent a specific functional and morphological class of layer VI neurons.

scholarly journals Temporo-nasally biased moving grating selectivity in mouse primary visual cortex

2019 ◽  
Author(s):  
Marie Tolkiehn ◽  
Simon R. Schultz
Keyword(s):  
Visual Cortex ◽  
Spatial Frequency ◽  
Primary Visual Cortex ◽  
Moving Objects ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
High Signal ◽  
Forward Movement ◽  
Upward Moving

AbstractOrientation tuning in mouse primary visual cortex (V1) has long been reported to have a random or “salt-and-pepper” organisation, lacking the structure found in cats and primates. Laminar in-vivo multi-electrode array recordings here reveal previously elusive structure in the representation of visual patterns in the mouse visual cortex, with temporo-nasally drifting gratings eliciting consistently highest neuronal responses across cortical layers and columns, whilst upward moving gratings reliably evoked the lowest activities. We suggest this bias in direction selectivity to be behaviourally relevant as objects moving into the visual field from the side or behind may pose a predatory threat to the mouse whereas upward moving objects do not. We found furthermore that direction preference and selectivity was affected by stimulus spatial frequency, and that spatial and directional tuning curves showed high signal correlations decreasing with distance between recording sites. In addition, we show that despite this bias in direction selectivity, it is possible to decode stimulus identity and that spatiotemporal features achieve higher accuracy in the decoding task whereas spike count or population counts are sufficient to decode spatial frequencies implying different encoding strategies.Significance statementWe show that temporo-nasally drifting gratings (i.e. opposite the normal visual flow during forward movement) reliably elicit the highest neural activity in mouse primary visual cortex, whereas upward moving gratings reliably evoke the lowest responses. This encoding may be highly behaviourally relevant, as objects approaching from the periphery may pose a threat (e.g. predators), whereas upward moving objects do not. This is a result at odds with the belief that mouse primary visual cortex is randomly organised. Further to this biased representation, we show that direction tuning depends on the underlying spatial frequency and that tuning preference is spatially correlated both across layers and columns and decreases with cortical distance, providing evidence for structural organisation in mouse primary visual cortex.

Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1

1992 ◽  
Vol 67 (6) ◽  
pp. 1437-1446 ◽  
Author(s):  
P. Girard ◽  
P. A. Salin ◽  
J. Bullier
Keyword(s):  
Receptive Field ◽  
Macaque Monkey ◽  
Direction Selectivity ◽  
Area 17 ◽  
Visual Responses ◽  
Area Mt ◽  
Reversible Inactivation ◽  
Mt Neurons ◽  
Preferred Direction ◽  
Blocking Index

1. Behavioral results in the monkey and clinical studies in human show remarkable residual visual capacities after a lesion of area V1. Earlier work by Rodman et al. demonstrated that visual activity can be recorded in the middle temporal area (MT) of the macaque monkey several weeks after a complete lesion of V1. These authors also tested the effect of a reversible block of area V1 on the visual responses of a small number of neurons in area MT and showed that most of these cells remain visually responsive. From the results of that study, however, it is difficult to assess the contribution of area 17 to the receptive-field selectivity of area MT neurons. To address this question, we have quantitatively measured the effects of a reversible inactivation of area 17 on the direction selectivity of MT neurons. 2. A circular part of the opercular region of area V1 was reversibly inactivated by cooling with a Peltier device. A microelectrode was positioned in the lower layers of V1 to control the total inactivation of that area. Eighty percent of the sites recorded in the retinotopically corresponding region of MT during inactivation of V1 were found to be visually responsive. The importance of the effect was assessed by calculating the blocking index (0 for no effect, 1 for complete inactivation). Approximately one-half of the quantitatively studied neurons gave a blocking index below 0.6, illustrating the strong residual responses recorded in many neurons. 3. Receptive-field properties were examined with multihistograms. It was found that, during inactivation of V1, the preferred direction changed for most neurons but remained close to the preferred direction or to its opposite in the control situation. During inactivation of V1, the average tuning curve of neurons became broader mostly because of strong reductions in the response to directions close to the preferred and nonpreferred. Very little change was observed in the responses for directions at 90 degrees to the optimal. These results are consistent with a model in which direction selectivity is present without an input from V1 but is reinforced by the spatial organization of this excitatory input. 4. Residual responses were found to be highly dependent on the state of anesthesia because they were completely abolished by the addition of 0.4-0.5% halothane to the ventilation gases. Finally, visual responses were recorded in area MT several hours after an acute lesion of area 17.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Orientation Tuning, But Not Direction Selectivity, Is Invariant to Temporal Frequency in Primary Visual Cortex

2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulus ◽  
Visual Processing ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
Orientation Contrast ◽  
Wide Range

The activity of neurons in primary visual cortex is influenced by the orientation, contrast, and temporal frequency of a visual stimulus. This raises the question of how these stimulus properties interact to shape neuronal responses. While past studies have shown that the bandwidth of orientation tuning is invariant to stimulus contrast, the influence of temporal frequency on orientation-tuning bandwidth is unknown. Here, we investigate the influence of temporal frequency on orientation tuning and direction selectivity in area 17 of ferret visual cortex. For both simple cells and complex cells, measures of orientation-tuning bandwidth (half-width at half-maximum response) are ∼20–25° across a wide range of temporal frequencies. Thus cortical neurons display temporal-frequency invariant orientation tuning. In contrast, direction selectivity is typically reduced, and occasionally reverses, at nonpreferred temporal frequencies. These results show that the mechanisms contributing to the generation of orientation tuning and direction selectivity are differentially affected by the temporal frequency of a visual stimulus and support the notion that stability of orientation tuning is an important aspect of visual processing.

A collicular visual cortex: Neocortical space for an ancient midbrain visual structure

Science ◽  
2019 ◽  
Vol 363 (6422) ◽  
pp. 64-69 ◽  
Author(s):  
Riccardo Beltramo ◽  
Massimo Scanziani
Keyword(s):  
Cerebral Cortex ◽  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Information ◽  
Cortical Area ◽  
Moving Objects ◽  
Visual Responses ◽  
Visual Cortical Area ◽  
Postrhinal Cortex ◽  
Visual Cortical

Visual responses in the cerebral cortex are believed to rely on the geniculate input to the primary visual cortex (V1). Indeed, V1 lesions substantially reduce visual responses throughout the cortex. Visual information enters the cortex also through the superior colliculus (SC), but the function of this input on visual responses in the cortex is less clear. SC lesions affect cortical visual responses less than V1 lesions, and no visual cortical area appears to entirely rely on SC inputs. We show that visual responses in a mouse lateral visual cortical area called the postrhinal cortex are independent of V1 and are abolished upon silencing of the SC. This area outperforms V1 in discriminating moving objects. We thus identify a collicular primary visual cortex that is independent of the geniculo-cortical pathway and is capable of motion discrimination.

Analysis of Direction Selectivity Arising from Recurrent Cortical Interactions

1998 ◽  
Vol 10 (2) ◽  
pp. 353-371 ◽  
Author(s):  
Paul Mineiro ◽  
David Zipser
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Detailed Comparison ◽  
Direction Selectivity ◽  
Dynamical Model ◽  
Physiological Data ◽  
Model Based ◽  
The Subject ◽  
Neuroscience Community

The relative contributions of feedforward and recurrent connectivity to the direction-selective responses of cells in layer IVB of primary visual cortex are currently the subject of debate in the neuroscience community. Recently, biophysically detailed simulations have shown that realistic direction-selective responses can be achieved via recurrent cortical interactions between cells with nondirection-selective feedforward input (Suarez et al., 1995; Maex & Orban, 1996). Unfortunately these models, while desirable for detailed comparison with biology, are complex and thus difficult to analyze mathematically. In this article, a relatively simple cortical dynamical model is used to analyze the emergence of direction-selective responses via recurrent interactions. A comparison between a model based on our analysis and physiological data is presented. The approach also allows analysis of the recurrently propagated signal, revealing the predictive nature of the implementation.

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