Orientation Tuning Bandwidth Research Articles

Orientation Tuning and End-stopping in Macaque V1 Studied with Two-photon Calcium Imaging.

Orientation tuning is a fundamental response property of V1 neurons and has been extensively studied with single-/multiunit recording and intrinsic signal optical imaging. Long-term 2-photon calcium imaging allows simultaneous recording of hundreds of neurons at single neuron resolution over an extended time in awake macaques, which may help elucidate V1 orientation tuning properties in greater detail. We used this new technology to study the microstructures of orientation functional maps, as well as population tuning properties, in V1 superficial layers of 5 awake macaques. Cellular orientation maps displayed horizontal and vertical clustering of neurons according to orientation preferences, but not tuning bandwidths, as well as less frequent pinwheels than previous estimates. The orientation tuning bandwidths were narrower than previous layer-specific single-unit estimates, suggesting more precise orientation selectivity. Moreover, neurons tuned to cardinal and oblique orientations did not differ in quantities and bandwidths, likely indicating minimal V1 representation of the oblique effect. Our experimental design also permitted rough estimates of length tuning. The results revealed significantly more end-stopped cells at a more superficial 150μm depth (vs. 300μm), but unchanged orientation tuning bandwidth with different length tuning. These results will help construct more precise models of V1 orientation processing.

Orientation Tuning of Correlated Activity in the Developing Lateral Geniculate Nucleus.

Neural circuits and the cells that comprise them undergo developmental changes in the spatial organization of their connections and in their temporal response properties. Within the lateral geniculate nucleus (LGN) of the dorsal thalamus, these changes have pronounced effects on the spatiotemporal receptive fields (STRFs) of neurons. An open and unresolved question is how STRF maturation affects stimulus-evoked correlated activity between pairs of LGN neurons during development. This is an important question to answer because stimulus-evoked correlated activity likely plays a role in establishing the specificity of thalamocortical connectivity and the receptive fields (RFs) of postsynaptic cortical neurons. Using multielectrode recording methods and white noise stimuli, we recorded neural activity from ensembles of LGN neurons in cats across early development. As expected, there was a progressive maturation of the spatial and temporal properties of visual responses. Using drifting bar stimuli and cross-correlation analysis, we also determined the orientation-tuning bandwidth of correlated activity between pairs of LGN neurons at different stages of development (Sillito and Jones, 2002; Andolina et al., 2007; Stanley et al., 2012; Kelly et al., 2014). Despite the larger RFs and slower responses of immature LGN neurons compared with mature neurons, our results show that correlated activity in the LGN was as tightly tuned for orientation early in development as it was in the adult. Closer examination revealed this age-invariant orientation tuning of correlated activity likely involves cellular mechanisms related to spike fatigue in young animals and a progressive decrease in response latency with development.SIGNIFICANCE STATEMENT Orientation tuning is a fundamental property of neurons in primary visual cortex. An important and unresolved question is how orientation tuning emerges during brain development. This study explores a potential mechanism for the establishment of orientation tuning based on correlated activity patterns among ensembles of maturing neurons in the lateral geniculate nucleus (LGN) of the thalamus. Results show that correlated activity between pairs of LGN neurons is more tightly tuned than predictions based simply on receptive field size, indicating that correlated activity has the properties needed to play an important role in the development of geniculocortical circuits and the emergence of cortical orientation tuning.

Alterations to global but not local motion processing in long-term ecstasy (MDMA) users

Growing evidence indicates that the main psychoactive ingredient in the illegal drug "ecstasy" (methylendioxymethamphetamine) causes reduced activity in the serotonin and gamma-aminobutyric acid (GABA) systems in humans. On the basis of substantial serotonin input to the occipital lobe, recent research investigated visual processing in long-term users and found a larger magnitude of the tilt aftereffect, interpreted to reflect broadened orientation tuning bandwidths. Further research found higher orientation discrimination thresholds and reduced long-range interactions in the primary visual area of ecstasy users. The aim of the present research was to investigate whether serotonin-mediated V1 visual processing deficits in ecstasy users extend to motion processing mechanisms. Forty-five participants (21 controls, 24 drug users) completed two psychophysical studies: A direction discrimination study directly measured local motion processing in V1, while a motion coherence task tested global motion processing in area V5/MT. "Primary" ecstasy users (n = 18), those without substantial polydrug use, had significantly lower global motion thresholds than controls [p = 0.027, Cohen's d = 0.78 (large)], indicating increased sensitivity to global motion stimuli, but no difference in local motion processing (p = 0.365). These results extend on previous research investigating the long-term effects of illicit drugs on visual processing. Two possible explanations are explored: defuse attentional processes may be facilitating spatial pooling of motion signals in users. Alternatively, it may be that a GABA-mediated disruption to V5/MT processing is reducing spatial suppression and therefore improving global motion perception in ecstasy users.

Altered visual perception in long-term ecstasy (MDMA) users

The present study investigated the long-term consequences of ecstasy use on visual processes thought to reflect serotonergic functions in the occipital lobe. Evidence indicates that the main psychoactive ingredient in ecstasy (methylendioxymethamphetamine) causes long-term changes to the serotonin system in human users. Previous research has found that amphetamine-abstinent ecstasy users have disrupted visual processing in the occipital lobe which relies on serotonin, with researchers concluding that ecstasy broadens orientation tuning bandwidths. However, other processes may have accounted for these results. The aim of the present research was to determine if amphetamine-abstinent ecstasy users have changes in occipital lobe functioning, as revealed by two studies: a masking study that directly measured the width of orientation tuning bandwidths and a contour integration task that measured the strength of long-range connections in the visual cortex of drug users compared to controls. Participants were compared on the width of orientation tuning bandwidths (26 controls, 12 ecstasy users, 10 ecstasy + amphetamine users) and the strength of long-range connections (38 controls, 15 ecstasy user, 12 ecstasy + amphetamine users) in the occipital lobe. Amphetamine-abstinent ecstasy users had significantly broader orientation tuning bandwidths than controls and significantly lower contour detection thresholds (CDTs), indicating worse performance on the task, than both controls and ecstasy + amphetamine users. These results extend on previous research, which is consistent with the proposal that ecstasy may damage the serotonin system, resulting in behavioral changes on tests of visual perception processes which are thought to reflect serotonergic functions in the occipital lobe.

A Multi-Stage Model for Fundamental Functional Properties in Primary Visual Cortex

Many neurons in mammalian primary visual cortex have properties such as sharp tuning for contour orientation, strong selectivity for motion direction, and insensitivity to stimulus polarity, that are not shared with their sub-cortical counterparts. Successful models have been developed for a number of these properties but in one case, direction selectivity, there is no consensus about underlying mechanisms. We here define a model that accounts for many of the empirical observations concerning direction selectivity. The model describes a single column of cat primary visual cortex and comprises a series of processing stages. Each neuron in the first cortical stage receives input from a small number of on-centre and off-centre relay cells in the lateral geniculate nucleus. Consistent with recent physiological evidence, the off-centre inputs to cortex precede the on-centre inputs by a small (∼4 ms) interval, and it is this difference that confers direction selectivity on model neurons. We show that the resulting model successfully matches the following empirical data: the proportion of cells that are direction selective; tilted spatiotemporal receptive fields; phase advance in the response to a stationary contrast-reversing grating stepped across the receptive field. The model also accounts for several other fundamental properties. Receptive fields have elongated subregions, orientation selectivity is strong, and the distribution of orientation tuning bandwidth across neurons is similar to that seen in the laboratory. Finally, neurons in the first stage have properties corresponding to simple cells, and more complex-like cells emerge in later stages. The results therefore show that a simple feed-forward model can account for a number of the fundamental properties of primary visual cortex.

Flicker adaptation of low-level cortical visual neurons contributes to temporal dilation.

Several seconds of adaptation to a flickered stimulus causes a subsequent brief static stimulus to appear longer in duration. Nonsensory factors, such as increased arousal and attention, have been thought to mediate this flicker-based temporal-dilation aftereffect. In this study, we provide evidence that adaptation of low-level cortical visual neurons contributes to this aftereffect. The aftereffect was significantly reduced by a 45° change in Gabor orientation between adaptation and test. Because orientation-tuning bandwidths are smaller in lower-level cortical visual areas and are approximately 45° in human V1, the result suggests that flicker adaptation of orientation-tuned V1 neurons contributes to the temporal-dilation aftereffect. The aftereffect was abolished when the adaptor and test stimuli were presented to different eyes. Because eye preferences are strong in V1 but diminish in higher-level visual areas, the eye specificity of the aftereffect corroborates the involvement of low-level cortical visual neurons. Our results suggest that flicker adaptation of low-level cortical visual neurons contributes to expanding visual duration. Furthermore, this temporal-dilation aftereffect dissociates from the previously reported temporal-compression aftereffect on the basis of the differences in their orientation and flicker-frequency selectivity, suggesting that the visual system possesses at least two distinct and potentially complementary mechanisms for adaptively coding perceived duration.

Where orientation tuning arises

Introduction: The neural circuitry underlying orientation selectivity, a fundamental question in vision, remains the center of controversy. Some advocate a modified feedforward model, originating in connections from LGN to V1, while others maintain that intracortical activity plays a crucial role in shaping selectivity. To test the role of intracortical activity in shaping orientation selectivity in humans, we employed TMS to attenuate cortical responses to an oriented stimulus and used noise masking to estimate orientation-tuning curves psychophysically. Methods: Prior to each block of experimental trials, we applied TMS pulses at 1 Hz continuously for 2.5 minutes, thereby depressing neural activity at a specific retinotopic site in early visual cortex including V1. In each trial, a filtered noise patch appeared inside or outside the visual region corresponding to the TMS site. A vertically oriented Gabor was embedded within the upper or lower portion of this noise patch, for which observers performed a 2AFC location discrimination task. To obtain psychophysical tuning functions, we used an orientation-bandpass noise masking procedure in which the noise and probe ranged from being identical in orientation, to the noise orientations being orthogonal to the Gabor probe. An adaptive procedure produced estimates of contrast thresholds for the probe embedded within varying orientation bandpass noise, yielding tuning curves for conditions when the stimuli appeared within or outside of the TMS site. Results and Conclusion: Contrast thresholds were elevated for several minutes following TMS (but only at the TMS site), confirming its effectiveness at depressing neural activity at that location. Orientation-tuning bandwidths, however, were unchanged by TMS stimulation. To confirm that TMS disrupts intracortical activity, we found that TMS weakens an illusion known to involve intracortical interactions. These results imply that orientation tuning is governed largely by thalamocortical feedforward signals, with intracortical activity contributing little to the sharpness of orientation tuning.

Neuronal Selectivity and Local Map Structure in Visual Cortex

The organization of primary visual cortex (V1) into functional maps makes individual cells operate in a variety of contexts. For instance, some neurons lie in regions of fairly homogeneous orientation preference (iso-orientation domains), while others lie in regions with a variety of preferences (e.g., pinwheel centers). We asked whether this diversity in local map structure correlates with the degree of selectivity of spike responses. We used a combination of imaging and electrophysiology to reveal that neurons in regions of homogeneous orientation preference have much sharper tuning. Moreover, in both monkeys and cats, a common principle links the structure of the orientation map, on the spatial scale of dendritic integration, to the degree of selectivity of individual cells. We conclude that neural computation is not invariant across the cortical surface. This finding must factor into future theories of receptive field wiring and map development.

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

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 approximately 20-25 degrees 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.

Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex.

Neurons in primary visual cortex are highly sensitive to the contrast, orientation, and temporal frequency of a visual stimulus. These three stimulus properties can be varied independently of one another, raising the question of how they interact to influence neuronal responses. We recorded from individual neurons in ferret primary visual cortex to determine the influence of stimulus contrast on orientation tuning, temporal-frequency tuning, and latency to visual response. Results show that orientation-tuning bandwidth is not affected by contrast level. Thus neurons in ferret visual cortex display contrast-invariant orientation tuning. Stimulus contrast does, however, influence the structure of orientation-tuning curves as measures of circular variance vary inversely with contrast for both simple and complex cells. This change in circular variance depends, in part, on a contrast-dependent change in the ratio of null to preferred orientation responses. Stimulus contrast also has an influence on the temporal-frequency tuning of cortical neurons. Both simple and complex cells display a contrast-dependent rightward shift in their temporal frequency-tuning curves that results in an increase in the highest temporal frequency needed to produce a half-maximum response (TF(50)). Results show that the degree of the contrast-dependent increase in TF(50) is similar for cortical neurons and neurons in the lateral geniculate nucleus (LGN) and indicate that subcortical mechanisms likely play a major role in establishing the degree of effect displayed by downstream neurons. Finally, results show that LGN and cortical neurons experience a contrast-dependent phase advance in their visual response. This phase advance is most pronounced for cortical neurons indicating a role for both subcortical and cortical mechanisms.

Independent component filters of natural images compared with simple cells in primary visual cortex.

Properties of the receptive fields of simple cells in macaque cortex were compared with properties of independent component filters generated by independent component analysis (ICA) on a large set of natural images. Histograms of spatial frequency bandwidth, orientation tuning bandwidth, aspect ratio and length of the receptive fields match well. This indicates that simple cells are well tuned to the expected statistics of natural stimuli. There is no match, however, in calculated and measured distributions for the peak of the spatial frequency response: the filters produced by ICA do not vary their spatial scale as much as simple cells do, but are fixed to scales close to the finest ones allowed by the sampling lattice. Possible ways to resolve this discrepancy are discussed.

The Tilt Illusion and the Orientation Bandwidth of Primary Level Filters

Models for pattern discrimination can be applied successfully to simple orientation discrimination tasks. However, the mechanisms underlying long-range spatial effects, such as the tilt illusion, are not well understood. The magnitude of the tilt illusion and its sensitivity to the polarity of the inducers were measured by means of tests with varying orientation bandwidths. The orientation tuning bandwidth of the primary-level filters, whose peak frequency is 1.7 cycles deg−1, was estimated in a 2AFC orientation-discrimination task. The luminance distribution of the stimulus was jointly normal. First, the orientation bandwidth of a single elongated test stimulus was increased by reducing its length-to-width ratio from 7.5:1 to 1.5:1. The orientation discrimination performance rapidly decreased after the ratio became less than 3.5:1, which is in good agreement with the estimates of the shape of the filters (Wilson, 1986 Vision Research26 453 – 469). These optimally shaped stimuli were used as inducers in the tilt illusion experiment. Six 20° tilted inducers were added around the test stimulus at the radial distance of 1.25 deg. When the length-to-width ratio of the test stimulus was varied as in the first experiment, the magnitude of the tilt illusion increased after the ratio was less than 3.5:1. However, the precision of the orientation discrimination when compared to the first experiment did not change. Changing the polarity of the inducers did not affect the illusion. The results suggest that the tilt effects of the inducers are not mediated by the primary-level filters. Rather, strengthening of the tilt illusion as the orientation bandwidth of the test stimulus increases suggests that long-range interactions between second-order orientation mechanisms might underlie the described phenomena.

Inactivation of the infragranular striate cortex broadens orientation tuning of supragranular visual neurons in the cat.

Intracortical inhibition is believed to enhance the orientation tuning of striate cortical neurons, but the origin of this inhibition is unclear. To examine the possible influence of ascending inhibitory projections from the infragranular layers of striate cortex on the orientation selectivity of neurons in the supragranular layers, we measured the spatiotemporal response properties of 32 supragranular neurons in the cat before, during, and after neural activity in the infragranular layers beneath the recorded cells was inactivated by iontophoretic administration of GABA. During GABA iontophoresis, the orientation tuning bandwidth of 15 (46.9%) supragranular neurons broadened as a result of increases in response amplitude to stimuli oriented about +/- 20 degrees away from the preferred stimulus angle. The mean (+/- SD) baseline orientation tuning bandwidth (half width at half height) of these neurons was 13.08 +/- 2.3 degrees. Their mean tuning bandwidth during inactivation of the infragranular layers increased to 19.59 +/- 2.54 degrees, an increase of 49.7%. The mean percentage increase in orientation tuning bandwidth of the individual neurons was 47.4%. Four neurons exhibited symmetrical changes in their orientation tuning functions, while 11 neurons displayed asymmetrical changes. The change in form of the orientation tuning functions appeared to depend on the relative vertical alignment of the recorded neuron and the infragranular region of inactivation. Neurons located in close vertical register with the inactivated infragranular tissue exhibited symmetric changes in their orientation tuning functions. The neurons exhibiting asymmetric changes in their orientation tuning functions were located just outside the vertical register. Eight of these 11 neurons also demonstrated a mean shift of 6.67 +/- 5.77 degrees in their preferred stimulus orientation. The magnitude of change in the orientation tuning functions increased as the delivery of GABA was prolonged. Responses returned to normal approximately 30 min after the delivery of GABA was discontinued. We conclude that inhibitory projections from neurons within the infragranular layers of striate cortex in cats can enhance the orientation selectivity of supragranular striate cortical neurons.

Direction and orientation selectivity of neurons in visual area MT of the macaque.

We recorded from single neurons in the middle temporal visual area (MT) of the macaque monkey and studied their direction and orientation selectivity. We also recorded from single striate cortex (V1) neurons in order to make direct comparisons with our observations in area MT. All animals were immobilized and anesthetized with nitrous oxide. Direction selectivity of 110 MT neurons was studied with three types of moving stimuli: slits, single spots, and random-dot fields. All of the MT neurons were found to be directionally selective using one or more of these stimuli. MT neurons exhibited a broad range of direction-tuning bandwidths to all stimuli (minimum = 32 degrees, maximum = 186 degrees, mean = 95 degrees). On average, responses were strongly unidirectional and of similar magnitude for all three stimulus types. Orientation selectivity of 89 MT neurons was studied with stationary flashed slits. Eighty-three percent were found to be orientation selective. Overall, orientation-tuning bandwidths were significantly narrower (mean = 64 degrees) than direction-tuning bandwidths for moving stimuli. Moreover, responses to stationary-oriented stimuli were generally smaller than those to moving stimuli. Direction selectivity of 55 V1 neurons was studied with moving slits; orientation selectivity of 52 V1 neurons was studied with stationary flashed slits. In V1, compared with MT, direction-tuning bandwidths were narrower (mean = 68 degrees). Moreover, V1 responses to moving stimuli were weaker, and bidirectional tuning was more common. The mean orientation-tuning bandwidth in V1 was also significantly narrower than that in MT (mean = 52 degrees), but the responses to stationary-oriented stimuli were of similar magnitude in the two areas. We examined the relationship between optimal direction and optimal orientation for MT neurons and found that 61% had an orientation preference nearly perpendicular to the preferred direction of motion, as is the case for all V1 neurons. However, another 29% of MT neurons had an orientation preference roughly parallel to the preferred direction. These observations, when considered together with recent reports claiming sensitivity of some MT neurons to moving visual patterns (39), suggest specific neural mechanisms underlying pattern-motion sensitivity in area MT. These results support the notion that area MT represents a further specialization over area V1 for stimulus motion processing. Furthermore, the marked similarities between direction and orientation tuning in area MT in macaque and owl monkey support the suggestion that these areas are homologues.