Leo Lui

Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity

In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3° to 70° eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell’s optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50°). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high‐speed (> 30°/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.

Spatial and temporal frequency selectivity of neurons in the middle temporal visual area of new world monkeys (Callithrix jacchus)

Information about the responses of neurons to the spatial and temporal frequencies of visual stimuli is important for understanding the types of computations being performed in different visual areas. We characterized the spatiotemporal selectivity of neurons in the middle temporal area (MT), which is deemed central for the processing of direction and speed of motion. Recordings obtained in marmoset monkeys using high‐contrast sine‐wave gratings as stimuli revealed that the majority of neurons had bandpass spatial and temporal frequency tuning, and that the selectivity for these parameters was largely separable. Only in about one‐third of the cells was inseparable spatiotemporal tuning detected, this typically being in the form of an increase in the optimal temporal frequency as a function of increasing grating spatial frequency. However, most of these interactions were weak, and only 10% of neurons showed spatial frequency‐invariant representation of speed. Cells with inseparable spatiotemporal tuning were most commonly found in the infragranular layers, raising the possibility that they form part of the feedback from MT to caudal visual areas. While spatial frequency tuning curves were approximately scale‐invariant on a logarithmic scale, temporal frequency tuning curves covering different portions of the spectrum showed marked and systematic changes. Thus, MT neurons can be reasonably described as similarly built spatial frequency filters, each covering a different dynamic range. The small proportion of speed‐tuned neurons, together with the laminar position of these units, are compatible with the idea that an explicit neural representation of speed emerges from computations performed in MT.

Representation of comparison signals in cortical area MT during a delayed direction discrimination task

Visually guided behavior often involves decisions that are based on evaluating stimuli in the context of those observed previously. Such decisions are made by monkeys comparing two consecutive stimuli, sample and test, moving in the same or opposite directions. We examined whether responses in the motion processing area MT during the comparison phase of this task (test) are modulated by the direction of the preceding stimulus (sample). This modulation, termed comparison signal, was measured by comparing responses to identical test stimuli on trials when it was preceded by sample moving in the same direction (S-trials) with trials when it was preceded by sample moving in a different direction (D-trials). The test always appeared in the neurons receptive field (RF), whereas sample could appear in the RF or in the contralateral visual field (remote sample). With sample in-RF, we found three types of modulation carried by different sets of neurons: early suppression on S-trials and late enhancement, one on S-trials, and the other on D-trials. Under these conditions, many neurons with and without comparison effects exhibited significant, choice-related activity. Response modulation was also present following the remote sample, even though the information about its direction could only reach MT indirectly via top-down influences. However, unlike on trials with in-RF sample, these signals were dominated by response suppression, shedding light on the contribution of top-down influences to the comparison effects. These results demonstrate that during the task requiring monkeys to compare two directions of motion, MT responses during the comparison phase of this task reflect similarities and differences between the two stimuli, suggesting participation in sensory comparisons. The nature of these signals provides insights into the operation of bottom-up and top-down influences involved in this process.

Development of non‐phosphorylated neurofilament protein expression in neurones of the New World monkey dorsolateral frontal cortex

We studied developmental changes in the expression of non‐phosphorylated neurofilament protein (NNF) (a marker of the structural maturation of pyramidal neurones) in the dorsolateral frontal cortex of marmoset monkeys, between embryonic day 130 and adulthood. Our focus was on cortical fields that send strong projections to extrastriate cortex, including the dorsal and ventral subdivisions of area 8A, area 46 and area 6d. For comparison, we also investigated the maturation of prefrontal area 9, which has few or no connections with visual areas. The timing of expression of NNF immunostaining in early life can be described as the result of the interaction of two developmental gradients. First, there is an anteroposterior gradient of maturation in the frontal lobe, whereby neurones in caudal areas express NNF earlier than those in rostral areas. Second, there is a laminar gradient, whereby the first NNF‐immunoreactive neurones emerge in layer V, followed by those in progressively more superficial parts of layer III. Following a peak in density of NNF‐immunopositive cell numbers in layer V at 2–3 months of age, there is a gradual decline towards adulthood. In contrast, the density of immunopositive cells in layer III continues to increase throughout the first postnatal year in area 6d and until late adolescence (> 1.5 years of age) in prefrontal areas. The present results support the view that the maturation of visual cognitive functions involves relatively late processes linked to structural changes in frontal cortical areas.

Single-unit responses to kinetic stimuli in New World monkey area V2: Physiological characteristics of cue-invariant neurones

In order to investigate the neural processes underlying figure-ground segregation on the basis of motion, we studied the responses of neurones in the second visual area (V2) of marmoset monkeys to stimuli that moved against dynamic textured backgrounds. The stimuli were either “solid” bars, which were uniformly darker or lighter than the background’s average, or kinetic (“camouflaged”) bars, formed by textural elements that matched the spatial and temporal modulation of the background. Camouflaged bars were rendered visible only by the coherent motion of their textural elements. Using solid bars, we subdivided the population of marmoset V2 neurones into motion-selective (uni- and bi-directional units, 73.3% of the sample) and weakly-biased (26.7%) subpopulations. The motion selective subpopulation was further subdivided into cue-invariant neurones (units which demonstrated a similar selectivity for the direction of motion of the solid and camouflaged bars) and non-cue-invariant neurones (units which showed selectivity to the direction of motion of solid bars, but had weak or pandirectional responses to camouflaged bars). Cells with cue-invariant responses to these stimuli were as common in V2 as in the primary visual area (V1; approximately 40% of the population). In V2, neurones with cue-invariant and non-cue-invariant motion selectivity formed distinct populations in terms of classical response properties: cue-invariant neurones were characterized by a sharp axis of motion selectivity and extensive length summation, while the majority of non-cue-invariant neurones had broader motion selectivity and were end-stopped. In the light of previous studies, these different constellations of classical response properties suggest a correlation with more traditionally recognized categories of V2 units and modular compartments. The responses of V2 cells to kinetic stimuli were slightly delayed relative to their responses to luminance-defined stimuli.

Breaking camouflage: responses of neurons in the middle temporal area to stimuli defined by coherent motion

Camouflaged animals remain inconspicuous only insofar as they remain static. This demonstrates that motion is a powerful cue for figure–ground segregation, allowing detection of moving objects even when their luminance and texture characteristics are matched to the background. We investigated the neural processes underlying this phenomenon by testing the responses of neurons in the middle temporal area (MT) to ‘camouflaged’ bars, which were rendered visible by motion. These responses were compared with those elicited by ‘solid’ bars, which also differed from background in terms of their mean luminance. Most MT neurons responded strongly to camouflaged bars, and signaled their direction of motion with precision, with direction‐tuning curves being only slightly wider than those measured with solid bars. However, the tuning of most MT cells to stimulus length and speed depended on the type of stimulus – in comparison with solid bars, responses to camouflaged bars typically showed more extensive length summation, weak end‐inhibition, and stronger attenuation at high speeds. Moreover, the emergence of direction selectivity was delayed in trials involving camouflaged bars, relative to solid bars. Comparison with results obtained in the first (V1) and second (V2) visual areas, using similar stimuli, indicates that neural computations performed in MT result in significantly stronger and more accurate signals about camouflaged objects, particularly in situations in which these are relatively large and slow moving. These computations are likely to represent an important step in enabling cue‐invariant perception of moving objects, particularly in biologically relevant situations.

Relationship between size summation properties, contrast sensitivity and response latency in the dorsomedial and middle temporal areas of the primate extrastriate cortex.

Analysis of the physiological properties of single neurons in visual cortex has demonstrated that both the extent of their receptive fields and the latency of their responses depend on stimulus contrast. Here, we explore the question of whether there are also systematic relationships between these response properties across different cells in a neuronal population. Single unit recordings were obtained from the middle temporal (MT) and dorsomedial (DM) extrastriate areas of anaesthetized marmoset monkeys. For each cell, spatial integration properties (length and width summation, as well as the presence of end- and side-inhibition within 15° of the receptive field centre) were determined using gratings of optimal direction of motion and spatial and temporal frequencies, at 60% contrast. Following this, contrast sensitivity was assessed using gratings of near-optimal length and width. In both areas, we found a relationship between spatial integration and contrast sensitivity properties: cells that summated over smaller areas of the visual field, and cells that displayed response inhibition at larger stimulus sizes, tended to show higher contrast sensitivity. In a sample of MT neurons, we found that cells showing longer latency responses also tended to summate over larger expanses of visual space in comparison with neurons that had shorter latencies. In addition, longer-latency neurons also tended to show less obvious surround inhibition. Interestingly, all of these effects were stronger and more consistent with respect to the selectivity for stimulus width and strength of side-inhibition than for length selectivity and end-inhibition. The results are partially consistent with a hierarchical model whereby more extensive receptive fields require convergence of information from larger pools of “feedforward” afferent neurons to reach near-optimal responses. They also suggest that a common gain normalization mechanism within MT and DM is involved, the spatial extent of which is more evident along the cell’s preferred axis of motion.

First- and second-order stimulus length selectivity in New World monkey striate cortex

Motion is a powerful cue for figure‐ground segregation, allowing the recognition of shapes even if the luminance and texture characteristics of the stimulus and background are matched. In order to investigate the neural processes underlying early stages of the cue‐invariant processing of form, we compared the responses of neurons in the striate cortex (V1) of anaesthetized marmosets to two types of moving stimuli: bars defined by differences in luminance, and bars defined solely by the coherent motion of random patterns that matched the texture and temporal modulation of the background. A population of form‐cue‐invariant (FCI) neurons was identified, which demonstrated similar tuning to the length of contours defined by first‐ and second‐order cues. FCI neurons were relatively common in the supragranular layers (where they corresponded to 28% of the recorded units), but were absent from layer 4. Most had complex receptive fields, which were significantly larger than those of other V1 neurons. The majority of FCI neurons demonstrated end‐inhibition in response to long first‐ and second‐order bars, and were strongly direction selective. Thus, even at the level of V1 there are cells whose variations in response level appear to be determined by the shape and motion of the entire second‐order object, rather than by its parts (i.e. the individual textural components). These results are compatible with the existence of an output channel from V1 to the ventral stream of extrastriate areas, which already encodes the basic building blocks of the image in an invariant manner.

Neural plasticity following lesions of the primate occipital lobe: The marmoset as an animal model for studies of blindsight.

For nearly a century it has been observed that some residual visually guided behavior can persist after damage to the primary visual cortex (V1) in primates. The age at which damage to V1 occurs leads to different outcomes, with V1 lesions in infancy allowing better preservation of visual faculties in comparison with those incurred in adulthood. While adult V1 lesions may still allow retention of some limited visual abilities, these are subconscious—a characteristic that has led to this form of residual vision being referred to as blindsight. The neural basis of blindsight has been of great interest to the neuroscience community, with particular focus on understanding the contributions of the different subcortical pathways and cortical areas that may underlie this phenomenon. More recently, research has started to address which forms of neural plasticity occur following V1 lesions at different ages, including work using marmoset monkeys. The relatively rapid postnatal development of this species, allied to the lissencephalic brains and well‐characterized visual cortex provide significant technical advantages, which allow controlled experiments exploring visual function in the absence of V1.

Auditory motion does not modulate spiking activity in the middle temporal and medial superior temporal visual areas

The integration of multiple sensory modalities is a key aspect of brain function, allowing animals to take advantage of concurrent sources of information to make more accurate perceptual judgments. For many years, multisensory integration in the cerebral cortex was deemed to occur only in high‐level “polysensory” association areas. However, more recent studies have suggested that cross‐modal stimulation can also influence neural activity in areas traditionally considered to be unimodal. In particular, several human neuroimaging studies have reported that extrastriate areas involved in visual motion perception are also activated by auditory motion, and may integrate audiovisual motion cues. However, the exact nature and extent of the effects of auditory motion on the visual cortex have not been studied at the single neuron level. We recorded the spiking activity of neurons in the middle temporal (MT) and medial superior temporal (MST) areas of anesthetized marmoset monkeys upon presentation of unimodal stimuli (moving auditory or visual patterns), as well as bimodal stimuli (concurrent audiovisual motion). Despite robust, direction selective responses to visual motion, none of the sampled neurons responded to auditory motion stimuli. Moreover, concurrent moving auditory stimuli had no significant effect on the ability of single MT and MST neurons, or populations of simultaneously recorded neurons, to discriminate the direction of motion of visual stimuli (moving random dot patterns with varying levels of motion noise). Our findings do not support the hypothesis that direct interactions between MT, MST and areas low in the hierarchy of auditory areas underlie audiovisual motion integration.