Functional maturation of the macaque's lateral geniculate nucleus.

Vision in infant primates is poor, but it is not known which structures in the eye or brain set the main limits to its development. We studied the visual response properties of 348 neurons recorded in the lateral geniculate nucleus (LGN) of macaque monkeys aged 1 week to adult. We measured spatial and temporal frequency tuning curves and contrast responses with drifting achromatic sinusoidal gratings. Even in animals as young as 1 week, the main visual response properties of neurons in the magnocellular (M) and parvocellular (P) divisions of the LGN were qualitatively normal, including the spatial organization of receptive fields and the characteristic response properties that differentiate M- and P-cells. At 1 and 4 weeks, spatial and temporal resolution were less than one-half of adult values, whereas contrast gain and peak response rates for optimal stimuli were about two-thirds of adult values. Adult levels were reached by 24 weeks. Analysis of correlations between S-potentials representing retinal inputs and LGN cells suggested that the LGN follows retinal input as faithfully in infants as in adults, implicating retinal development as the main driving force in LGN development. Comparisons with previously published psychophysical data and ideal observer models suggest that the relatively modest changes in LGN responses during maturation impose no significant limits on visual performance. In contrast to previous studies, we conclude that these limits are set by neural development in the visual cortex, not in or peripheral to the LGN.

Time course and time-distance relationships for surround suppression in macaque V1 neurons.

Iso-orientation surround suppression is a powerful form of visual contextual modulation in which a stimulus of the preferred orientation of a neuron placed outside the classical receptive field (CRF) of the neuron suppresses the response to stimuli within the CRF. This suppression is most often attributed to orientation-tuned signals that propagate laterally across the cortex, activating local inhibition. By studying the temporal properties of surround suppression, we have uncovered characteristics that challenge standard notions of surround suppression. We found that the latency of suppression depended on its strength. Across cells, strong suppression arrived on average 30 msec earlier than weak suppression, and suppression sometimes arrived faster than the excitatory CRF response. We compared the relative latency of CRF response onset and offset with the relative latency of suppression onset and offset. Response onset was delayed relative to response offset in the CRF but not in the surround. This is not the expected result if neurons targeted by suppression are like those that generate it. We examined the time course of suppression as a function of distance of the surround stimulus from the CRF and found that suppression was predominantly sustained for nearby stimuli and predominantly transient for distant stimuli. By comparing the latency of suppression for nearby and distant stimuli, we found that orientation-tuned suppression could effectively propagate across 6 - 8 mm of cortex at approximately 1 m/sec. This is considerably faster than expected for horizontal cortical connections previously implicated in surround suppression. We offer refinements to circuits for surround suppression that account for these results and describe how feedback from cells with large CRFs can account for the rapid propagation of suppression within V1.

Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons.

The responsiveness of neurons in V1 is modulated by stimuli placed outside their classical receptive fields. This nonclassical surround provides input from a larger portion of the visual scene than originally thought, permitting integration of information at early levels in the visual processing stream. Signals from the surround have been reported variously to be suppressive and facilitatory, selective and unselective. We tested the specificity of influences from the surround by studying the interactions between drifting sinusoidal gratings carefully confined to conservatively defined center and surround regions. We found that the surround influence was always suppressive when the surround grating was at the neuron's preferred orientation. Suppression tended to be stronger when the surround grating also moved in the neuron's preferred direction, rather than its opposite. When the orientation in the surround was 90 degrees from the preferred orientation (orthogonal), suppression was weaker, and facilitation was sometimes evident. The tuning of surround signals therefore tended to match the tuning of the center, though the tuning of the surround was somewhat broader. The tuning of suppression also depended on the contrast of the center grating-when the center grating was reduced in contrast, orthogonal surround stimuli became relatively more suppressive. We also found evidence for the tuning of the surround being dependent to some degree on the stimulus used in the center-suppression was often stronger for a given center stimulus when the parameters of the surround grating matched the parameters of the center grating even when the center grating was not itself of the optimal direction or orientation. We also explored the spatial distribution of surround influence and found an orderly relationship between the orientation of grating patches presented to regions of the surround and the position of greatest suppression. When surround gratings were oriented parallel to the preferred orientation of the receptive field, suppression was strongest at the receptive field ends. When surround gratings were orthogonal, suppression was strongest on the flanks. We conclude that the surround has complex effects on responses from the classical receptive field. We suggest that the underlying mechanism of this complexity may involve interactions between relatively simple center and surround mechanisms.

Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons.

Information is integrated across the visual field to transform local features into a global percept. We now know that V1 neurons provide more spatial integration than originally thought due to the existence of their nonclassical inhibitory surrounds. To understand spatial integration in the visual cortex, we have studied the nature and extent of center and surround influences on neuronal response. We used drifting sinusoidal gratings in circular and annular apertures to estimate the sizes of the receptive field's excitatory center and suppressive surround. We used combinations of stimuli inside and outside the receptive field to explore the nature of the surround influence on the receptive field center as a function of the relative and absolute contrast of stimuli in the two regions. We conclude that the interaction is best explained as a divisive modulation of response gain by signals from the surround. We then develop a receptive field model based on the ratio of signals from Gaussian-shaped center and surround mechanisms. We show that this model can account well for the variations in receptive field size with contrast that we and others have observed and for variations in size with the state of contrast adaptation. The model achieves this success by simple variations in the relative gain of the two component mechanisms of the receptive field. This model thus offers a parsimonious explanation of a variety of phenomena involving changes in apparent receptive field size and accounts for these phenomena purely in terms of two receptive field mechanisms that do not themselves change in size. We used the extent of the center mechanism in our model as an indicator of the spatial extent of the central excitatory portion of the receptive field. We compared the extent of the center to measurements of horizontal connections within V1 and determined that horizontal intracortical connections are well matched in extent to the receptive field center mechanism. Input to the suppressive surround may come in part from feedback signals from higher areas.

The timing of response onset and offset in macaque visual neurons.

We used fast, pseudorandom temporal sequences of preferred and antipreferred stimuli to drive neuronal firing rates rapidly between minimal and maximal across the visual system. Stimuli were tailored to the preferences of cells recorded in the lateral geniculate nucleus (magnocellular and parvocellular), primary visual cortex (simple and complex), and the extrastriate motion area MT. We found that cells took longer to turn on (to increase their firing rate) than to turn off (to reduce their rate). The latency difference (onset minus offset) varied from several to tens of milliseconds across cell type and stimulus class and was correlated with spontaneous or driven firing rates for most cell classes. The delay for response onset depended on the nature of the stimulus present before the preferred stimulus appeared, and may result from persistent inhibition caused by antipreferred stimuli or from suppression that followed the offset of the preferred stimulus. The onset delay showed three distinct types of dependence on the temporal sequence of stimuli across classes of cells, implying that suppression may accumulate or wear off with time. Onset latency is generally longer, can be more variable, and has marked stimulus dependence compared with offset latency. This suggests an important role for offset latency in assessing the speed of information transmission in the visual system and raises the possibility that signal offsets provide a timing reference for visual processing. We discuss the origin of the delay in onset latency compared with offset latency and consider how it may limit the utility of certain feedforward circuits.

Differential metabolic activity in the striosome and matrix compartments of the rat striatum during natural behaviors.

The striosome and matrix compartments of the striatum are clearly identified by their neurochemical expression patterns and anatomical connections. To determine whether these compartments are distinguishable functionally, we used [14C]deoxyglucose metabolic mapping in the rat and tested whether neutral behavioral states (free movement, gentle restraint, and focal tactile stimulation under gentle restraint) were associated with regions of high metabolic activity in the matrix, in striosomes, or in both. We identified metabolic peaks in the striatum by means of image analysis, striosome-matrix boundaries by [3H]naloxone binding, and primary somatosensory corticostriatal input clusters by injections of anterograde tracer into electrophysiologically identified sites in SI. Peak metabolic activity was primarily confined to the matrix compartment under each behavioral condition. These findings show that during relatively neutral behavioral conditions the balance of activity between the two compartments favors the matrix and suggest that this balance is present in the striatum as part of normal behavior and processing of afferent activity.