Spatial Receptive Field Properties Research Articles

Poster Session I: Gain, not changes in spatial receptive field properties, improves task performance in a neural network attention model.

Attention allows us to focus sensory processing on behaviorally relevant aspects of the visual world. One potential mechanism of attention is a change in the gain of sensory responses. However, changing gain at early stages could have multiple downstream consequences for visual processing. Which, if any, of these effects can account for the benefits of attention for detection and discrimination? Using a model of primate visual cortex we document how a Gaussian-shaped gain modulation results in changes to spatial tuning properties. Forcing the model to use only these changes failed to produce any benefit in task performance. Instead, we found that gain alone was both necessary and sufficient to explain category detection and discrimination during attention. Our results show how gain can give rise to changes in receptive fields which are not necessary for enhancing task performance.

Gain, not concomitant changes in spatial receptive field properties, improves task performance in a neural network attention model.

Attention allows us to focus sensory processing on behaviorally relevant aspects of the visual world. One potential mechanism of attention is a change in the gain of sensory responses. However, changing gain at early stages could have multiple downstream consequences for visual processing. Which, if any, of these effects can account for the benefits of attention for detection and discrimination? Using a model of primate visual cortex we document how a Gaussian-shaped gain modulation results in changes to spatial tuning properties. Forcing the model to use only these changes failed to produce any benefit in task performance. Instead, we found that gain alone was both necessary and sufficient to explain category detection and discrimination during attention. Our results show how gain can give rise to changes in receptive fields which are not necessary for enhancing task performance.

Spatial selectivity in adaptation to gaze direction.

A person's focus of attention is conveyed by the direction of their eyes and face, providing a simple visual cue fundamental to social interaction. A growing body of research examines the visual mechanisms that encode the direction of another person's gaze as we observe them. Here we investigate the spatial receptive field properties of these mechanisms, by testing the spatial selectivity of sensory adaptation to gaze direction. Human observers were adapted to faces with averted gaze presented in one visual hemifield, then tested in their perception of gaze direction for faces presented in the same or opposite hemifield. Adaptation caused strong, repulsive perceptual aftereffects, but only for faces presented in the same hemifield as the adapter. This occurred even though adapting and test stimuli were in the same external location across saccades. Hence, there was clear evidence for retinotopic adaptation and a relative lack of either spatiotopic or spatially invariant adaptation. These results indicate that adaptable representations of gaze direction in the human visual system have retinotopic spatial receptive fields. This strategy of coding others' direction of gaze with positional specificity relative to one's own eye position may facilitate key functions of gaze perception, such as socially cued shifts in visual attention.

Learning Spatiotemporal Properties of Hippocampal Place Cells.

It is well known that hippocampal place cells have spatiotemporal properties, namely, that they generally respond to a single spatial location of a small environment, and they also display the temporal response property of theta phase precession, namely, that the phase of spiking relative to the theta wave shifts from the late phase to early phase as the animal crosses the place field. Grid cells in Layer II of the medial entorhinal cortex (MEC) also have spatiotemporal properties similar to hippocampal place cells, except that grid cells respond to multiple spatial locations that form a hexagonal pattern. Because the EC is the upstream area that projects strongly to the hippocampus, a number of EC-hippocampus learning models have been proposed to explain how the spatial receptive field properties of place cells emerge via synaptic plasticity. However, the question of how the phase precession properties of place cells and grid cells are related has remained unclear. This study shows how theta phase precession in hippocampal place cells can emerge from MEC input as a result of synaptic plasticity, demonstrating that a learning model based on non-negative sparse coding can account for both the spatial and temporal properties of hippocampal place cells. Although both MEC grid cells and other EC spatial cells contribute to the spatial properties of hippocampal place cells, it is the MEC grid cells that predominantly determine the temporal response properties of hippocampal place cells displayed here.

Optogenetic activation of corticogeniculate feedback stabilizes response gain and increases information coding in LGN neurons.

In spite of their anatomical robustness, it has been difficult to establish the functional role of corticogeniculate circuits connecting primary visual cortex with the lateral geniculate nucleus of the thalamus (LGN) in the feedback direction. Growing evidence suggests that corticogeniculate feedback does not directly shape the spatial receptive field properties of LGN neurons, but rather regulates the timing and precision of LGN responses and the information coding capacity of LGN neurons. We propose that corticogeniculate feedback specifically stabilizes the response gain of LGN neurons, thereby increasing their information coding capacity. Inspired by early work by McClurkin et al. (1994), we manipulated the activity of corticogeniculate neurons to test this hypothesis. We used optogenetic methods to selectively and reversibly enhance the activity of corticogeniculate neurons in anesthetized ferrets while recording responses of LGN neurons to drifting gratings and white noise stimuli. We found that optogenetic activation of corticogeniculate feedback systematically reduced LGN gain variability and increased information coding capacity among LGN neurons. Optogenetic activation of corticogeniculate neurons generated similar increases in information encoded in LGN responses to drifting gratings and white noise stimuli. Together, these findings suggest that the influence of corticogeniculate feedback on LGN response precision and information coding capacity could be mediated through reductions in gain variability.

Role of Feedback Connections in Central Visual Processing.

The physiological response properties of neurons in the visual system are inherited mainly from feedforward inputs. Interestingly, feedback inputs often outnumber feedforward inputs. Although they are numerous, feedback connections are weaker, slower, and considered to be modulatory, in contrast to fast, high-efficacy feedforward connections. Accordingly, the functional role of feedback in visual processing has remained a fundamental mystery in vision science. At the core of this mystery are questions about whether feedback circuits regulate spatial receptive field properties versus temporal responses among target neurons, or whether feedback serves a more global role in arousal or attention. These proposed functions are not mutually exclusive, and there is compelling evidence to support multiple functional roles for feedback. In this review, the role of feedback in vision will be explored mainly from the perspective of corticothalamic feedback. Further generalized principles of feedback applicable to corticocortical connections will also be considered.

Refinement of Spatial Receptive Fields in the Developing Mouse Lateral Geniculate Nucleus Is Coordinated with Excitatory and Inhibitory Remodeling.

Receptive field properties of individual visual neurons are dictated by the precise patterns of synaptic connections they receive, including the arrangement of inputs in visual space and features such as polarity (On vs Off). The inputs from the retina to the lateral geniculate nucleus (LGN) in the mouse undergo significant refinement during development. However, it is unknown how this refinement corresponds to the establishment of functional visual response properties. Here we conducted in vivo and in vitro recordings in the mouse LGN, beginning just after natural eye opening, to determine how receptive fields develop as excitatory and feedforward inhibitory retinal afferents refine. Experiments used both male and female subjects. For in vivo assessment of receptive fields, we performed multisite extracellular recordings in awake mice. Spatial receptive fields at eye-opening were >2 times larger than in adulthood, and decreased in size over the subsequent week. This topographic refinement was accompanied by other spatial changes, such as a decrease in spot size preference and an increase in surround suppression. Notably, the degree of specificity in terms of On/Off and sustained/transient responses appeared to be established already at eye opening and did not change. We performed in vitro recordings of the synaptic responses evoked by optic tract stimulation across the same time period. These recordings revealed a pairing of decreased excitatory and increased feedforward inhibitory convergence, providing a potential mechanism to explain the spatial receptive field refinement.SIGNIFICANCE STATEMENT The development of precise patterns of retinogeniculate connectivity has been a powerful model system for understanding the mechanisms underlying the activity-dependent refinement of sensory systems. Here we link the maturation of spatial receptive field properties in the lateral geniculate nucleus (LGN) to the remodeling of retinal and inhibitory feedforward convergence onto LGN neurons. These findings should thus provide a starting point for testing the cell type-specific plasticity mechanisms that lead to refinement of different excitatory and inhibitory inputs, and for determining the effect of these mechanisms on the establishment of mature receptive fields in the LGN.

Local Order within Global Disorder: Synaptic Architecture of Visual Space

Substantial evidence at the subcellular level indicates that the spatial arrangement of synaptic inputs onto dendrites could play a significant role in cortical computations, but how synapses of functionally defined cortical networks are arranged within the dendrites of individual neurons remains unclear. Here we assessed one-dimensional spatial receptive fields of individual dendritic spines within individual layer 2/3 neuron dendrites. Spatial receptive field properties of dendritic spines were strikingly diverse, with no evidence of large-scale topographic organization. At a fine scale, organization was evident: neighboring spines separated by less than 10μm shared similar spatial receptive field properties andexhibited a distance-dependent correlation in sensory-driven and spontaneous activity patterns. Fine-scale dendritic organization was supported by the fact that functional groups of spines defined by dimensionality reduction of receptive field properties exhibited non-random dendritic clustering. Our results demonstrate that functional synaptic clustering is a robust feature existing at a local spatial scale. VIDEO ABSTRACT.

Circuit Mechanisms of a Retinal Ganglion Cell with Stimulus-Dependent Response Latency and Activation Beyond Its Dendrites

Center-surround antagonism has been used as the canonical model to describe receptive fields of retinal ganglion cells (RGCs) for decades. We describe a newly identified RGC type in the mouse, called the ON delayed (OND) RGC, with receptive field properties that deviate from center-surround organization. Responding with an unusually long latency to light stimulation, OND RGCs respond earlier as the visual stimulus increases in size. Furthermore, OND RGCs are excited by light falling far beyond their dendrites. We unravel details of the circuit mechanisms behind these phenomena, revealing new roles for inhibition in controlling both temporal and spatial receptive field properties. The non-canonical receptive field properties of the OND RGC-integration of long temporal and large spatial scales-suggest that unlike typical RGCs, it may encode a slowly varying, global property of the visual scene.

Spatial receptive field properties of rat retinal ganglion cells

The rat is a popular animal model for vision research, yet there is little quantitative information about the physiological properties of the cells that provide its brain with visual input, the retinal ganglion cells. It is not clear whether rats even possess the full complement of ganglion cell types found in other mammals. Since such information is important for evaluating rodent models of visual disease and elucidating the function of homologous and heterologous cells in different animals, we recorded from rat ganglion cells in vivo and systematically measured their spatial receptive field (RF) properties using spot, annulus, and grating patterns. Most of the recorded cells bore likeness to cat X and Y cells, exhibiting brisk responses, center-surround RFs, and linear or nonlinear spatial summation. The others resembled various types of mammalian W cell, including local-edge-detector cells, suppressed-by-contrast cells, and an unusual type with an ON-OFF surround. They generally exhibited sluggish responses, larger RFs, and lower responsiveness. The peak responsivity of brisk-nonlinear (Y-type) cells was around twice that of brisk-linear (X-type) cells and several fold that of sluggish cells. The RF size of brisk-linear and brisk-nonlinear cells was indistinguishable, with average center and surround diameters of 5.6 ± 1.3 and 26.4 ± 11.3 deg, respectively. In contrast, the center diameter of recorded sluggish cells averaged 12.8 ± 7.9 deg. The homogeneous RF size of rat brisk cells is unlike that of cat X and Y cells, and its implication regarding the putative roles of these two ganglion cell types in visual signaling is discussed.

Spatial receptive field properties of lateral geniculate cells in the owl monkey (Aotus azarae) at different contrasts: a comparative study

Several physiological properties of owl monkey lateral geniculate nucleus (LGN) cells were studied to verify whether its nocturnal habit has an influence on the organization of its subcortical visual system. Receptive field (RF) dimensions were measured using drifting gratings and bipartite field stimuli. We found that owl monkey cells LGN have larger RFs and were on average more non-linear than those of diurnal monkeys. But, as in other anthropoids, there is an increase in RF centre size with increasing eccentricity, and there is a limited correlation between these centre sizes and retinal ganglion cell dendritic tree sizes. The influence of contrast on sizes and peak sensitivities of RF centres and surrounds and on the response phases was studied. Both the sizes and peak sensitivities of the RF centres and surrounds decrease as contrast increases. As a result, the responses to low spatial frequency stimuli saturate with increasing contrast. Estimates of contrasts at half-maximal responses confirm the presence of saturation. It was found that the magnocellular cells saturate more strongly than parvocellular cells. The response phase increases with increasing contrast. These data resemble those obtained in the common marmoset, indicating that these are basic features of the primate visual system. We conclude that during evolution and as an adaptation to a nocturnal lifestyle, cells in the owl monkey LGN display an increased spatial integration in comparison with diurnal primate species, without a change in the basic organization common to the primate subcortical visual system.

Brainstem modulation of visual response properties of single cells in the dorsal lateral geniculate nucleus of cat.

The dorsal lateral geniculate nucleus (dLGN) transmits visual signals from the retina to the cortex. In the dLGN the antagonism between the centre and the surround of the receptive fields is increased through intrageniculate inhibitory mechanisms. Furthermore, the transmission of signals through the dLGN is modulated in a state-dependent manner by input from various brainstem nuclei including an area in the parabrachial region (PBR) containing cholinergic cells involved in the regulation of arousal and sleep. Here, we studied the effects of increased PBR input on the spatial receptive field properties of cells in the dLGN. We made simultaneous single-unit recordings of the input to the cells from the retina (S-potentials) and the output of the cells to the cortex (action potentials) to determine spatial receptive field modifications generated in the dLGN. State-dependent modulation of the spatial receptive field properties was studied by electrical stimulation of the PBR. The results showed that PBR stimulation had only a minor effect on the modifications of the spatial receptive field properties generated in the dLGN. The PBR-evoked effects could be described mainly as increased response gain. This suggested that the spatial modifications of the receptive field occurred at an earlier stage of processing in the dLGN than the PBR-controlled gain regulation, such that the PBR input modulates the gain of the spatially modified signals. We propose that the spatial receptive field modifications occur at the input to relay cells through the synaptic triades between retinal afferents, inhibitory interneurone dendrites, and relay cell dendrites and that the gain regulation is related to postsynaptic cholinergic effects on the relay cells.

Brain stem modulation of spatial receptive field properties of single cells in the dorsal lateral geniculate nucleus of the cat.

1. We studied the effect of electrical stimulation of the peribrachial region (PBR) in the brain stem on the visual response of single cells in the dorsal lateral geniculate nucleus (dLGN) to a light slit presented in a series of positions across the receptive field. The response was plotted against slit position, giving a spatial receptive field profile. 2. PBR stimulation markedly increased the visual response. In the middle of the receptive field center, the absolute response increase was considerably larger than in the peripheral parts of the receptive field or than the increase of spontaneous activity. The PBR stimulation also led to a small increase of the diameter of the receptive field center. 3. The maximum steepness of the receptive field profile for the dLGN cells increased by PBR stimulation. We suggest that the visual resolution in the dLGN cell is directly related to this maximal slope of the receptive field profile rather than to the width of the receptive field center. This would mean that increased input from the PBR, as presumably occurs during arousal, increases the visual resolution of the dLGN cells. 4. For some of the cells we could record S-potentials (slow potentials) in addition to action potentials. This allowed us to directly compared the receptive field center size of a dLGN cell with that of its retinal input. For these cells, the center size was considerably reduced by the geniculate relay. During PBR stimulation, the center size of these cells also increased slightly, but even in this condition it was reduced compared with the retinal input. The maximal slope of the receptive field profile in the dLGN cell during PBR stimulation was larger than for the retinal input. 5. We also examined the effect of ionophoretical application of acetylcholine (ACh) and bicuculline methchloride (BMC) on the spatial receptive field properties of dLGN cells. The effects of ACh were similar to those of PBR stimulation. Application of BMC, on the other hand, made the receptive field profile more similar to that of retinal ganglion cells.

Frequency sensitivity and directional hearing in the gleaning bat, Plecotus auritus (Linnaeus 1758).

1. The neural audiogram of the common long-eared bat, Plecotus auritus was recorded from the inferior colliculus (IC). The most sensitive best frequency (BF) thresholds for single neurones are below 0 dB SPL between 7-20 kHz, reaching a best value of -20 dB SPL between 12-20 kHz. The lower and upper limits of hearing occur at 3 kHz and 63 kHz, respectively, based on BF thresholds at 80 dB SPL. BF threshold sensitivities are about 10 dB SPL between 25-50 kHz, corresponding to the energy band of the sonar pulse (26-78 kHz). The tonotopic organization of the central nucleus of the IC (ICC) reveals that neurones with BFs below 20 kHz are disproportionately represented, occupying about 30% of ICC volume, occurring in the more rostral and lateral regions of the nucleus. 2. The acoustical gain of the external ear reaches a peak of about 20 dB between 8-20 kHz. The gain of the pinna increases rapidly above 4 kHz, to a peak of about 15 dB at 7-12 kHz. The pinna gain curve is similar to that of a simple, finite length acoustic horn; expected horn gain is calculated from the average dimensions of the pinna. 3. The directional properties of the external ear are based on sound diffraction by the pinna mouth, which, to a first approximation, is equivalent to an elliptical opening due to the elongated shape of the pinna. The spatial receptive field properties for IC neurones are related to the directional properties of the pinna. The position of the acoustic axis of the pinna and the best position (BP) of spatial receptive fields are both about 25 degrees from the midline between 8-30 kHz but approach the midline to 8 degrees at 45 kHz. In elevation, the acoustic axis and the BP of receptive fields move upwards by 20 degrees between 9-25 kHz, remaining stationary for frequencies up to 60 kHz. 4. The extremely high auditory sensitivity shown by the audiogram and the directionality of hearing are discussed in terms of the adaptation of the auditory system to low frequencies and the role of a large pinna in P. auritus. The functional significance of low frequency hearing in P. auritus is discussed in relation to hunting for prey by listening and is compared to other gleaning species.

Spatial and temporal determinants of directionally selective velocity preference in cat striate cortex neurons

1. Direction-selective properties of neurons in cat striate cortex (area 17) were studied with flashed and continuously moving bar stimuli. Receptive fields were characterized by measurement of static and dynamic parameters, which were correlated with the velocity preference exhibited by the same cells. 2. Each neuron was found to be direction selective to a limited range of velocities. This behavior was characterized by measuring the optimal velocity (Vopt) to elicit responses in the preferred and null directions that were maximally distinct. 3. A bar stimulus flashed sequentially at two nearby locations in the receptive field also produced direction-selective behavior, which was characterized by an optimal displacement (Dopt) to drive maximally distinct responses in the preferred versus null directions. 4. The static spatial receptive field properties were quantified by measurement of the receptive field size (2 sigma) and the spatial subunit wavelength (lambda). The latter quantity was measured as twice the separation between adjacent ON and OFF regions in simple cells and as twice the optimal separation for lateral inhibition between two simultaneously flashed bars in complex cells. 5. Direction-selective velocity preference for continuously moving stimuli, Vopt, was found to be highly correlated with lambda and with the Dopt for 2-flash motion; Vopt was also correlated to a lesser degree with 2 sigma. These results suggest a fundamental linkage between spatial frequency preference, velocity preference, and spatial tuning to 2-flash motion. 6. The range of measured direction-selective velocity preference values (Vopt) spanned about a 100-fold range, whereas the corresponding values of Dopt or lambda spanned substantially smaller ranges. This discrepancy suggested that the dynamic range of velocity preference among cortical neurons might be determined jointly by the measured spatial properties and by a temporal property that covaries with the measured spatial properties. 7. Temporal properties of striate cortical neurons were assessed from responses to flashed stimuli having a prolonged duration ("step responses"). Neurons typically responded in the following manner: after some latency (L), a transient rise in spike frequency occurred, which then adapted to some sustained level. The adaptation dynamics (extent of sustained vs. transient behavior) were quantified by the first-order time constant (AT) of the adaptation decay, and by the ratio of initial transient rise to final sustained level [adaptation ratio (AR)].(ABSTRACT TRUNCATED AT 400 WORDS)

Responses of single units in the monkey superior colliculus to moving stimuli.

1. Single unit responses of pan-directional cells to moving and stationary flashing stimuli were studied in the superficial layers of the superior colliculus in paralysed, anaesthetized rhesus monkeys. The aim of this study was to see how far cell responses to moving stimuli fit in with what would be expected from their responses to stationary flashing stimuli. 2. Both the leading and the trailing edge of a moving stimulus evoke a transient response. If the diameter of moving light spots is increased the strength of the leading edge response increases, reaches a maximum and decreases to a constant value which is similar to the behaviour of the on response when the diameter of flashing spots is increased. The strength of the trailing edge response increases and reaches the same strength as that of the leading edge response. If the width of a long moving slit is increased, the strength of the leading edge response is the same at all slit widths, while the strength of the trailing edge response shows a course similar to that of the trailing edge response if the spot diameter is increased. If the length of a wide moving slit is increased both the leading and the trailing edge responses decrease. These results indicate that the strength of both leading and trailing edge responses is dependent on the degree the inhibitory surround is activated. 3. The leading and the trailing edge of a stimulus evoke their responses at the same position in the receptive field independent of the direction of movement. 4. Increasing the velocity of a moving stimulus shows that in general the leading edge response is present up to higher velocities than the trailing edge response independent of the sign of contrast. The burst duration to moving stimuli decreases with increasing stimulus velocity and appears to be determined by the time a moving edge is present in the receptive field centre. When this time becomes shorter than 10--20 ms, the burst duration for moving stimuli is constant and about the same as for flashing stimuli. This indicates that, although spatial receptive field properties can vary considerably, temporal receptive field properties show a strong similarity among different units. 5. The response latencies to light and dark moving edges are the same, which in turn are about equal to the response latencies to stationary flashing stimuli. 6. Stimulation experiments show that the general response characteristics to moving stimuli can be predicted by using a set of receptive field parameters derived from responses to stationary flashing stimuli. The most important variable of moving stimuli appears to be the period of time a moving contour is present within the receptive field centre, besides the degree of activation of the inhibitory surround.