Temporal interactions in the cat visual system. II. Suppressive and facilitatory effects in the lateral geniculate nucleus

Extracellular responses were recorded from single neurons in the lateral geniculate nucleus (LGN) of the cat during presentation of pairs of brief visual stimuli identical to those that produce orientation-selective paired-pulsed suppression in the visual cortex. LGN neurons also show paired-pulse suppression, but the suppression is not orientation selective, and it occurs only for short interstimulus intervals (ISIs; usually less than 200 msec). At longer ISIs, most LGN neurons show a period of facilitation. Thus, the paired-pulse suppression in the LGN cannot account for that seen in the visual cortex. Paired-pulse suppression in the LGN was found to be enhanced by stimulation of the receptive field surround. LGN neurons also showed a second type of suppression, termed "offset suppression," which consisted of a more long-lasting suppression of spontaneous activity following the offset of an excitatory visual stimulus. The suppression of spontaneous activity was accompanied by a reduction of the antidromic excitability, assessed by stimulating LGN axons within the cortex or optic radiation. Unlike paired-pulsed suppression, offset suppression was not enhanced by increased stimulation of the receptive field surround. Paired-pulse suppression and offset suppression are most likely due to different mechanisms because they have different time courses and depend differently on the spatial properties of the stimuli. Functionally, paired-pulse suppression may be related to the reduced visual sensitivity that accompanies eye movements, while offset suppression may serve to enhance temporal contrast.     

Temporal interactions in the cat visual system. I. Orientation-selective suppression in the visual cortex

The perception of a visual contour depends on the spatial and temporal context in which it is viewed. Interactions between visual contours are believed to underlie a wide range of perceptual phenomena, including geometric illusions and aftereffects, contrast adaptation, and visual masking. The physiological mechanisms that might underlie such interactions were studied in the visual cortex of the cat by recording responses of single neurons to pairs of brief stationary stimuli that were separated in time. The results revealed a long-lasting, orientation-selective suppression, termed "paired-pulse suppression," which was strongest at the cell's preferred orientation, but which was more broadly tuned for orientation than the excitatory response of the cell. Although the strength and duration of the suppression varied widely, some degree of response reduction was present in most cells studied. The function of this suppression may be to regulate the gain with which visual inputs are transmitted to cortical neurons, thus preventing response saturation and positive feedback.     

Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum

The activity of single neurons was recorded in the tail of the caudate nucleus and adjoining part of the ventral putamen, which receive projections from the inferior temporal visual cortex, in order to investigate the functions of these regions. Of 195 neurons analyzed in two macaque monkeys, 109 (56%) responded to visual stimuli, with latencies of 90-150 ms for the majority of the neurons. The neurons responded to a limited range of complex visual stimuli, and in some cases responded to simpler stimuli such as bars and edges. Typically (in 75% of cases) the neurons habituated rapidly, within 1-8 exposures, to each visual stimulus, but remained responsive to other visual stimuli with a different pattern. This habituation was orientation specific, in that the neurons responded to the same pattern shown in an orthogonal orientation. The habituation was also relatively short-term, in that at least partial dishabituation to one stimulus could be produced by a single intervening presentation of a different visual stimulus. These neurons were relatively unresponsive in a visual discrimination task, having habituated to the stimuli which had been presented in the task on many previous trials. It is suggested on the basis of these results and other studies that these neurons are involved in pattern-specific habituation to repeated visual stimuli, and in attention an orientation to a changed visual stimulus pattern. Changes in attention and orientation to stimuli as a result of damage to the striatum and its afferent and efferent pathways may arise in part because of damage to neurons with responses of this type.     

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles

Information processing in the vertebrate brain is thought to be mediated through distributed neural networks, but it is still unclear how sensory stimuli are encoded and detected by these networks, and what role synaptic inhibition plays in this process. Here we used a collision avoidance behavior in Xenopus tadpoles as a model for stimulus discrimination and recognition. We showed that the visual system of the tadpole is selective for behaviorally relevant looming stimuli, and that the detection of these stimuli first occurs in the optic tectum. By comparing visually guided behavior, optic nerve recordings, excitatory and inhibitory synaptic currents, and the spike output of tectal neurons, we showed that collision detection in the tadpole relies on the emergent properties of distributed recurrent networks within the tectum. We found that synaptic inhibition was temporally correlated with excitation, and did not actively sculpt stimulus selectivity, but rather it regulated the amount of integration between direct inputs from the retina and recurrent inputs from the tectum. Both pharmacological suppression and enhancement of synaptic inhibition disrupted emergent selectivity for looming stimuli. Taken together these findings suggested that, by regulating the amount of network activity, inhibition plays a critical role in maintaining selective sensitivity to behaviorally‐relevant visual stimuli.     

Disparity sensitivity of neurons in monkey extrastriate area MST.

We tested the disparity sensitivity of neurons from the medial superior temporal area (MST) in awake behaving monkeys. While the monkey looked at a fixation spot on a screen in front of it, random dot stimuli moved in the preferred direction of the cell under study, and the disparity of the dots made the stimuli appear to move in a frontoparallel plane in front of, on, or behind the screen. Over 90% of the 272 neurons studied were sensitive to the disparity of the visual stimulus. Of those disparity-sensitive cells, 95% were most responsive either to near stimuli (stimuli with crossed disparities appearing to move in front of the screen) or to far stimuli (stimuli with uncrossed disparities appearing to move behind the screen). In a smaller sample of the disparity-sensitive cells, we found cells whose preferred direction of stimulus motion reversed as the disparity of the stimulus reversed. For example, a cell that responded best to rightward motion for near stimuli responded best to leftward motion for far stimuli. We found that 40% of the disparity-sensitive cells had this disparity-dependent direction selectivity. This disparity-dependent direction selectivity was maintained over the entire range of speeds tested (6-56 degrees/sec). We tested whether the disparity sensitivity of the neurons indicated the distance of the stimulus from the screen where the monkey was fixating (relative depth) or the distance of the stimulus from the monkey (absolute depth) by having the monkey fixate at different depths in front of or behind the screen. For most MST neurons, the changes in vergence did not alter the disparity response, indicating that the disparity sensitivity of these neurons conveyed information on depth relative to the plane of fixation. We conclude that the disparity characteristics of cells in the dorsomedial MST are those expected of a system serving primarily coarse rather than fine stereopsis. The correlation between disparity selectivity and direction selectivity in these neurons, as well as their other properties, suggests a role in signaling the direction of self-motion of the observer through the environment.     

Orientation selectivity in rat primary visual cortex emerges earlier with low‐contrast and high‐luminance stimuli

In natural vision, rapid and sustained variations in luminance and contrast change the reliability of information available about a visual scene, and markedly affect both neuronal and behavioural responses. The hallmark property of neurons in primary visual cortex (V1), orientation selectivity, is unaffected by changes in stimulus contrast, but it remains unclear how sustained differences in mean luminance and contrast affect the time‐course of orientation selectivity, and the amount of information that neurons carry about orientation. We used reverse correlation with characterize the temporal dynamics of orientation selectivity in rat V1 neurons under four luminance‐contrast conditions. We show that orientation selectivity and mutual information between neuronal responses and stimulus orientation are invariant to contrast or mean luminance. Critically, the time‐course of the emergence of orientation selectivity was affected by both factors; response latencies were longer for low‐ than high‐luminance gratings, and surprisingly, response latencies were also longer for high‐ than low‐contrast gratings. Modelling suggests that luminance‐modulated changes in feedforward gain, in combination with hyperpolarization caused by high contrasts can account for our physiological data. The hyperpolarization at high contrasts may increase signal‐to‐noise ratios, whereas a more depolarized membrane may lead to greater sensitivity to weak stimuli.     

Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal

In a previous study (Rodman et al., 1989), we found that many neurons in the middle temporal area (MT) of the macaque monkey remain visually responsive and directionally selective after striate cortex lesions or cooling. In the present study, we examined the effects of superior colliculus (SC) lesions and combined lesions of striate cortex and the SC on the visual properties of MT neurons. Removal of the SC alone had no effect on the proportion of visually responsive cells, strength of direction selectivity and direction tuning, orientation tuning, receptive field size, or binocularity in MT. There was, however, a slight increase in response strength to both stationary and moving slit stimuli. In contrast to the minor effects of SC lesions alone, addition of an SC lesion to striate cortex damage abolished all visual responsiveness in area MT. The results indicate that pathways damaged by the SC lesion are not necessary for most of the properties of MT neurons found in the intact animal, although these pathways are capable of sustaining considerable visual responsiveness and direction selectivity when striate input is removed.     

Contrast invariance of orientation tuning in the lateral geniculate nucleus of the feline visual system

Responses of most neurons in the primary visual cortex of mammals are markedly selective for stimulus orientation and their orientation tuning does not vary with changes in stimulus contrast. The basis of such contrast invariance of orientation tuning has been shown to be the higher variability in the response for low‐contrast stimuli. Neurons in the lateral geniculate nucleus (LGN), which provides the major visual input to the cortex, have also been shown to have higher variability in their response to low‐contrast stimuli. Parallel studies have also long established mild degrees of orientation selectivity in LGN and retinal cells. In our study, we show that contrast invariance of orientation tuning is already present in the LGN. In addition, we show that the variability of spike responses of LGN neurons increases at lower stimulus contrasts, especially for non‐preferred orientations. We suggest that such contrast‐ and orientation‐sensitive variability not only explains the contrast invariance observed in the LGN but can also underlie the contrast‐invariant orientation tuning seen at the level of the primary visual cortex.     

Visual orientation and directional selectivity through thalamic synchrony

Thalamic neurons respond to visual scenes by generating synchronous spike trains on the timescale of 10-20 ms that are very effective at driving cortical targets. Here we demonstrate that this synchronous activity contains unexpectedly rich information about fundamental properties of visual stimuli. We report that the occurrence of synchronous firing of cat thalamic cells with highly overlapping receptive fields is strongly sensitive to the orientation and the direction of motion of the visual stimulus. We show that this stimulus selectivity is robust, remaining relatively unchanged under different contrasts and temporal frequencies (stimulus velocities). A computational analysis based on an integrate-and-fire model of the direct thalamic input to a layer 4 cortical cell reveals a strong correlation between the degree of thalamic synchrony and the nonlinear relationship between cortical membrane potential and the resultant firing rate. Together, these findings suggest a novel population code in the synchronous firing of neurons in the early visual pathway that could serve as the substrate for establishing cortical representations of the visual scene.     

Stimulus-selective properties of inferior temporal neurons in the macaque

Previous studies have reported that some neurons in the inferior temporal (IT) cortex respond selectively to highly specific complex objects. In the present study, we conducted the first systematic survey of the responses of IT neurons to both simple stimuli, such as edges and bars, and highly complex stimuli, such as models of flowers, snakes, hands, and faces. If a neuron responded to any of these stimuli, we attempted to isolate the critical stimulus features underlying the response. We found that many of the responsive neurons responded well to virtually every stimulus tested. The remaining, stimulus-selective cells were often selective along the dimensions of shape, color, or texture of a stimulus, and this selectivity was maintained throughout a large receptive field. Although most IT neurons do not appear to be "detectors" for complex objects, we did find a separate population of cells that responded selectively to faces. The responses of these cells were dependent on the configuration of specific face features, and their selectivity was maintained over changes in stimulus size and position. A particularly high incidence of such cells was found deep in the superior temporal sulcus. These results indicate that there may be specialized mechanisms for the analysis of faces in IT cortex.     

Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors

One of the most impressive features of the central nervous system is its ability to process information from a variety of stimuli to produce an integrated, comprehensive representation of the external world. In the present study, the temporal disparity among combinations of different sensory stimuli was shown to be a critical factor influencing the integration of multisensory stimuli by superior colliculus neurons. Several temporal principles that govern multisensory integration were revealed: (1) maximal levels of response enhancement were generated by overlapping the peak discharge periods evoked by each modality; (2) the magnitude of this enhancement decayed monotonically to zero as the peak discharge periods became progressively more temporally disparate; (3) with further increases in temporal disparity, the same stimulus combinations that previously produced enhancement could often produce depression; and (4) these kinds of interactions could frequently be predicted from the discharge trains initiated by each stimulus alone. Since multisensory superior colliculus neurons project to premotor areas of the brain stem and spinal cord that control the orientation of the receptor organs (eyes, pinnae, head), they are believed to influence attentive and orientation behaviors. Therefore, it is likely that the temporal relationships of different environmental stimuli that control the activity of these neurons are also a powerful determinant of superior colliculus-mediated attentive and orientation behaviors.     

Surround suppression sharpens orientation tuning in the cat primary visual cortex

In the primary visual cortex (V1), the response of a neuron to stimulation of its classical receptive field (CRF) is suppressed by concurrent stimulation of the extraclassical receptive field (ECRF), a phenomenon termed 'surround suppression'. It is also known that the orientation tuning of V1 neurons becomes sharper as the size of the stimulus increases beyond the CRF. However, there have been few quantitative investigations of the relationship between sharpening of orientation tuning and surround suppression. We examined this relationship in 73 V1 neurons recorded from anesthetized and paralysed cats using sinusoidal grating patches as stimuli. We found that sharpening of orientation tuning was significantly correlated with the strength of surround suppression for large stimuli that cover both CRF and ECRF. Furthermore, simulation analysis using a variety of tuning widths and most suppressive orientation of orientation-tuned surround suppression demonstrated that broadly orientation-tuned surround suppression sharpens orientation tuning for large gratings without shift in optimal orientation. Our findings suggest that one of the functional roles of surround suppression in V1 is enhancement of orientation discrimination for large and uniformly patterned objects.     

Response properties of local field potentials and neighboring single neurons in awake primary visual cortex

Recordings from local field potentials (LFPs) are becoming increasingly common in research and clinical applications, but we still have a poor understanding of how LFP stimulus selectivity originates from the combined activity of single neurons. Here, we systematically compared the stimulus selectivity of LFP and neighboring single-unit activity (SUA) recorded in area primary visual cortex (V1) of awake primates. We demonstrate that LFP and SUA have similar stimulus preferences for orientation, direction of motion, contrast, size, temporal frequency, and even spatial phase. However, the average SUA had 50 times better signal-to-noise, 20% higher contrast sensitivity, 45% higher direction selectivity, and 15% more tuning depth than the average LFP. Low LFP frequencies (<30 Hz) were most strongly correlated with the spiking frequencies of neurons with nonlinear spatial summation and poor orientation/direction selectivity that were located near cortical current sinks (negative LFPs). In contrast, LFP gamma frequencies (>30 Hz) were correlated with a more diverse group of neurons located near cortical sources (positive LFPs). In summary, our results indicate that low- and high-frequency LFP pool signals from V1 neurons with similar stimulus preferences but different response properties and cortical depths.     

Inhibition of milk ejection by a visual stimulus in lactating rats: Implication of the pineal gland

The effect of visual and auditory stimuli on milk ejection during suckling was studied in normal and pinealectomized lactating rats. The photic and auditory stimuli were applied to each mother for 10s every 20s during the 30 min suckling period. Both stimuli inhibited milk ejection without altering the nursing behavior. In mothers kept in complete darkness or in which the visual stimulus shone continously during the suckling period, milk ejection was not affected. The inhibition of milk ejection is therefore produced by the light on-off sequence. In lactating rats exposed to the stimulus during 3 consecutive days, a significant inhibition of milk ejection was obtained each day. A normal milk-ejection response ocurred in both non-stimulated pinealectomized and in stimulated pinealectomized lactating rats. Pinealectomy did not prevent the inhibitory effect of the sound stimulus. Treatment with methysergide prevented the inhibition of milk ejection induced by the visual stimulus but did not prevent the inhibitory effect of the auditory stimulus. It seems that the pineal gland mediates an inhibitory visual reflex acting on oxytocin release and milk ejection.     

Spatial sensitivity of macaque inferior temporal neurons

Recent findings in dorsal visual stream areas and computational work raise the question whether neurons at the end station of the ventral visual stream can code for stimulus position. The authors provide the first detailed, quantitative data on the spatial sensitivity of neurons in the anterior part of the inferior temporal cortex (area TE) in awake, fixating monkeys. They observed a large variation in receptive field (RF) size (ranging from 2.8 degrees to 26 degrees ). TE neurons differed in their optimal position, with a bias toward the foveal position. Moreover, the RF profiles of most TE neurons could be fitted well with a two-dimensional Gaussian function. Most neurons had only one region of high sensitivity and showed a smooth decline in sensitivity toward more distal positions. In addition, the authors investigated some of the possible determinants of such spatial sensitivity. First, testing with low-pass filtered versions of the stimuli revealed that the general preference for the foveal position and the size of the RFs was not due simply to TE neurons receiving input with a lower spatial resolution at more eccentric positions. The foveal position was still preferred after intense low-pass filtering. Second, although an increase in stimulus size consistently broadened spatial sensitivity profiles, it did not change the qualitative features of these profiles. Moreover, size selectivity of TE neurons was generally position invariant. Overall, the results suggest that TE neurons can code for the position of stimuli in the central region of the visual field.     

Visual responses of neurons in the dorsolateral amygdala of the alert monkey

There is evidence that the inferotemporal visual cortex in the monkey projects to the amygdala, and evidence that damage to this region impairs the learning of associations between visual stimuli and reward or punishment. In recordings made in the amygdala to determine whether or not visual responses were found, and if so how they were affected by the significance of the visual stimuli, neurons were found in the dorsolateral part of the amygdala with visual responses which in most cases were sustained while the animal looked at effective visual stimuli. The latency of the responses was 100 to 140 ms or more. The majority (85%) of these neurons responded more strongly to some stimuli than to others, but physical factors which accounted for the responses of the neurons, such as shape, size, orientation, color, or texture, could not usually be identified. Although 22 (19.5%) of these neurons responded primarily to food objects, the responses were not uniquely food-related. Furthermore, although some neurons responded in a visual discrimination test to a visual stimulus which indicated reward, and not to a visual stimulus which indicated saline, only minor modifications of the magnitude of the neuronal responses to the stimuli were obtained when the reward-related significance of the stimuli was reversed. The visual responses of these amygdaloid neurons were thus intermediate in some respects between those of neurons in the inferotemporal cortex, which are not affected by the significance of visual stimuli, and those of neurons in a region to which the amygdala projects, the lateral hypothalamus and substantia innominata, where neurons respond to visual stimuli associated with food reward.     

Visual Familiarity Induced 5-Hz Oscillations and Improved Orientation and Direction Selectivities in V1

Neural oscillations play critical roles in information processing, communication between brain areas, learning, and memory. We have recently discovered that familiar visual stimuli can robustly induce 5-Hz oscillations in the primary visual cortex (V1) of awake mice after the visual experience. To gain more mechanistic insight into this phenomenon, we used in vivo patch-clamp recordings to monitor the subthreshold activity of individual neurons during these oscillations. We analyzed the visual tuning properties of V1 neurons in naive and experienced mice to assess the effect of visual experience on the orientation and direction selectivity. Using optogenetic stimulation through the patch pipette in vivo, we measured the synaptic strength of specific intracortical and thalamocortical projections in vivo in the visual cortex before and after the visual experience. We found 5-Hz oscillations in membrane potential (V_m) and firing rates evoked in single neurons in response to the familiar stimulus, consistent with previous studies. Following the visual experience, the average firing rates of visual responses were reduced while the orientation and direction selectivities were increased. Light-evoked EPSCs were significantly increased for layer 5 (L5) projections to other layers of V1 after the visual experience, while the thalamocortical synaptic strength was decreased. In addition, we developed a computational model that could reproduce 5-Hz oscillations with enhanced neuronal selectivity following synaptic plasticity within the recurrent network and decreased feedforward input.SIGNIFICANCE STATEMENT Neural oscillations at around 5 Hz are involved in visual working memory and temporal expectations in primary visual cortex (V1). However, how the oscillations modulate the visual response properties of neurons in V1 and their underlying mechanism is poorly understood. Here, we show that these oscillations may alter the orientation and direction selectivity of the layer 2/3 (L2/3) neurons and correlate with the synaptic plasticity within V1. Our computational recurrent network model reproduces all these observations and provides a mechanistic framework for studying the role of 5-Hz oscillations in visual familiarity.     

Perceptual inference predicts contextual modulations of sensory responses

Sensory receptive fields (RFs) vary as a function of stimulus properties and measurement methods. Previous stimuli or surrounding stimuli facilitate, suppress, or change the selectivity of sensory neurons' responses. Here, we propose that these spatiotemporal contextual dependencies are signatures of efficient perceptual inference and can be explained by a single neural mechanism, input targeted divisive inhibition. To respond both selectively and reliably, sensory neurons should behave as active predictors rather than passive filters. In particular, they should remove input they can predict ("explain away") from the synaptic inputs to all other neurons. This implies that RFs are constantly and dynamically reshaped by the spatial and temporal context, while the true selectivity of sensory neurons resides in their "predictive field." This approach motivates a reinvestigation of sensory representations and particularly the role and specificity of surround suppression and adaptation in sensory areas.     

Emergence of Nonlinear Mixed Selectivity in Prefrontal Cortex after Training

Neurons in the PFC are typically activated by different cognitive tasks, and also by different stimuli and abstract variables within these tasks. A single neuron''s selectivity for a given stimulus dimension often changes depending on its context, a phenomenon known as nonlinear mixed selectivity (NMS). It has previously been hypothesized that NMS emerges as a result of training to perform tasks in different contexts. We tested this hypothesis directly by examining the neuronal responses of different PFC areas before and after male monkeys were trained to perform different working memory tasks involving visual stimulus locations and/or shapes. We found that training induces a modest increase in the proportion of PFC neurons with NMS exclusively for spatial working memory, but not for shape working memory tasks, with area 9/46 undergoing the most significant increase in NMS cell proportion. We also found that increased working memory task complexity, in the form of simultaneously storing location and shape combinations, does not increase the degree of NMS for stimulus shape with other task variables. Lastly, in contrast to the previous studies, we did not find evidence that NMS is predictive of task performance. Our results thus provide critical insights on the representation of stimuli and task information in neuronal populations, in working memory.SIGNIFICANCE STATEMENT How multiple types of information are represented in working memory remains a complex computational problem. It has been hypothesized that nonlinear mixed selectivity allows neurons to efficiently encode multiple stimuli in different contexts, after subjects have been trained in complex tasks. Our analysis of prefrontal recordings obtained before and after training monkeys to perform working memory tasks only partially agreed with this prediction, in that nonlinear mixed selectivity emerged for spatial but not shape information, and mostly in mid-dorsal PFC. Nonlinear mixed selectivity also displayed little modulation across either task complexity or correct performance. These results point to other mechanisms, in addition to nonlinear mixed selectivity, representing complex information about stimulus and task context in neuronal activity.     

Interactions of visual and auditory mossy fiber inputs in the paraflocculus of the rat: a gating action of multimodal inputs

We have demonstrated previously that visual and auditory inputs reach the rat paraflocculus via dorsolateral pontine gray from the secondary regions of the visual and auditory cortices. It has also been demonstrated that mossy fiber responses can be evoked to physiological acoustic stimuli in unanesthetized preparations. In this study, we investigated the interaction of auditory and visual inputs in the paraflocculus. Activity of parafloccular neurons was recorded in immobilized, locally anesthetized hooded rats. Selected images and tones were presented to animals. Orientation, position, and velocity of visual stimuli and different parameters of acoustic stimuli were controlled by a computer. Visual and auditory stimuli were also presented in combination or in different temporal sequences. We discovered that visual and auditory stimuli have coextensive termination zones in paraflocculus, and influence the same neurons in 60% of the cases. Combined auditory and visual stimuli produced synergistic responses in parafloccular neurons in comparison with single modality stimuli. Augmentation of responses could be observed even when one of the stimuli was subthreshold and did not alter per se the neuronal activity. Our findings suggest that within the cerebro-cerebellar system, subthreshold inputs are capable of powerful control over the neuronal activity and may alter responses to subsequent stimuli when properly biased by inputs from paired modalities.