Auditory-prefrontal axonal connectivity in the macaque cortex: quantitative assessment of processing streams.

Primate sensory systems subserve complex neurocomputational functions. Consequently, these systems are organised anatomically in a distributed fashion, commonly linking areas to form specialised processing streams. Each stream is related to a specific function, as evidenced from studies of the visual cortex, which features rather prominent segregation into spatial and non-spatial domains. It has been hypothesised that other sensory systems, including auditory, are organised in a similar way on the cortical level. Recent studies offer rich qualitative evidence for the dual stream hypothesis. Here we provide a new paradigm to quantitatively uncover these patterns in the auditory system, based on an analysis of multiple anatomical studies using multivariate techniques. As a test case, we also apply our assessment techniques to more ubiquitously-explored visual system. Importantly, the introduced framework opens the possibility for these techniques to be applied to other neural systems featuring a dichotomised organisation, such as language or music perception.

Optogenetic assessment of horizontal interactions in primary visual cortex.

Columnar organization of orientation selectivity and clustered horizontal connections linking orientation columns are two of the distinctive organizational features of primary visual cortex in many mammalian species. However, the functional role of these connections has been harder to characterize. Here we examine the extent and nature of horizontal interactions in V1 of the tree shrew using optical imaging of intrinsic signals, optogenetic stimulation, and multi-unit recording. Surprisingly, we find the effects of optogenetic stimulation depend primarily on distance and not on the specific orientation domains or axes in the cortex, which are stimulated. In addition, across a wide range of variation in both visual and optogenetic stimulation we find linear addition of the two inputs. These results emphasize that the cortex provides a rich substrate for functional interactions that are not limited to the orientation-specific interactions predicted by the monosynaptic distribution of horizontal connections.

Terminator disparity contributes to stereo matching for eye movements and perception.

In the context of motion detection, the endings (or terminators) of 1-D features can be detected as 2-D features, affecting the perceived direction of motion of the 1-D features (the barber-pole illusion) and the direction of tracking eye movements. In the realm of binocular disparity processing, an equivalent role for the disparity of terminators has not been established. Here we explore the stereo analogy of the barber-pole stimulus, applying disparity to a 1-D noise stimulus seen through an elongated, zero-disparity, aperture. We found that, in human subjects, these stimuli induce robust short-latency reflexive vergence eye movements, initially in the direction orthogonal to the 1-D features, but shortly thereafter in the direction predicted by the disparity of the terminators. In addition, these same stimuli induce vivid depth percepts, which can only be attributed to the disparity of line terminators. When the 1-D noise patterns are given opposite contrast in the two eyes (anticorrelation), both components of the vergence response reverse sign. Finally, terminators drive vergence even when the aperture is defined by a texture (as opposed to a contrast) boundary. These findings prove that terminators contribute to stereo matching, and constrain the type of neuronal mechanisms that might be responsible for the detection of terminator disparity.

Receptive field positions in area MT during slow eye movements.

Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas.

Attention narrows position tuning of population responses in V1.

When attention is directed to a region of space, visual resolution at that location flexibly adapts, becoming sharper to resolve fine-scale details or coarser to reflect large-scale texture and surface properties. By what mechanism does attention improve spatial resolution? An improved signal-to-noise ratio (SNR) at the attended location contributes, because of retinotopically specific signal gain. Additionally, attention could sharpen position tuning at the neural population level, so that adjacent objects activate more distinct regions of the visual cortex. A dual mechanism involving both signal gain and sharpened position tuning would be highly efficient at improving visual resolution, but there is no direct evidence that attention can narrow the position tuning of population responses. Here, we compared the spatial spread of the fMRI BOLD response for attended versus ignored stimuli. The activity produced by adjacent stimuli overlapped less when subjects were attending at their locations versus attending elsewhere, despite a stronger peak response with attention. Our results show that even as early as primary visual cortex (V1), spatially directed attention narrows the tuning of population-coded position representations.

Functional geometry of the horizontal connectivity in the primary visual cortex.

We present a geometrical model of the functional architecture of the primary visual cortex. In particular we describe the geometric structure of connections found both in neurophysiological and psychophysical experiments, modeling both co-axial and trans-axial excitatory connections. The model shows what could be the deep structure for both boundary and figure completion and for morphological structures such as the medial axis of a shape.

Evidence for joint encoding of motion and disparity in human visual perception.

Electrophysiological recordings have established that motion and disparity signals are jointly encoded by subpopulations of neurons in visual cortex. However, the question of whether these neurons play a perceptual role has proven challenging and remains open. To answer this question we combined two powerful psychophysical techniques: perceptual adaptation and reverse correlation. Our results provide a detailed picture of how visual information about motion and disparity is processed by human observers, and how this processing is modified by prolonged sensory stimulation. We were able to isolate two perceptual components: a separable component, supported by separate motion and disparity signals, and an inseparable joint component, supported by motion and disparity signals that are concurrently represented at the level of the same neural mechanism. Both components are involved in the perception of stimuli containing motion and disparity information in line with the known existence of corresponding neuronal subpopulations in visual cortex.

Receptive field shift and shrinkage in macaque middle temporal area through attentional gain modulation.

Selective attention is the top-down mechanism to allocate neuronal processing resources to the most relevant subset of the information provided by an organism's sensors. Attentional selection of a spatial location modulates the spatial-tuning characteristics (i.e., the receptive fields of neurons in macaque visual cortex). These tuning changes include a shift of receptive field centers toward the focus of attention and a narrowing of the receptive field when the attentional focus is directed into the receptive field. Here, we report that when attention is directed into versus of receptive fields of neurons in the middle temporal visual area (area MT), the magnitude of the shift of the spatial-tuning functions is positively correlated with a narrowing of spatial tuning around the attentional focus. By developing and applying a general attentional gain model, we show that these nonmultiplicative attentional modulations of basic neuronal-tuning characteristics could be a direct consequence of a spatially distributed multiplicative interaction of a bell-shaped attentional spotlight with the spatially fined-grained sensory inputs of MT neurons. Additionally, the model lets us estimate the spatial spread of the attentional top-down signal impinging on visual cortex. Consistent with psychophysical reports, the estimated size of the "spotlight of attention" indicates a coarse spatial resolution of attention. These results illustrate how spatially specific nonmultiplicative attentional changes of neuronal-tuning functions can be the result of multiplicative gain modulation affecting sensory neurons in a widely distributed region in cortical space.

Adaptive coding of visual information in neural populations.

Our perception of the environment relies on the capacity of neural networks to adapt rapidly to changes in incoming stimuli. It is increasingly being realized that the neural code is adaptive, that is, sensory neurons change their responses and selectivity in a dynamic manner to match the changes in input stimuli. Understanding how rapid exposure, or adaptation, to a stimulus of fixed structure changes information processing by cortical networks is essential for understanding the relationship between sensory coding and behaviour. Physiological investigations of adaptation have contributed greatly to our understanding of how individual sensory neurons change their responses to influence stimulus coding, yet whether and how adaptation affects information coding in neural populations is unknown. Here we examine how brief adaptation (on the timescale of visual fixation) influences the structure of interneuronal correlations and the accuracy of population coding in the macaque (Macaca mulatta) primary visual cortex (V1). We find that brief adaptation to a stimulus of fixed structure reorganizes the distribution of correlations across the entire network by selectively reducing their mean and variability. The post-adaptation changes in neuronal correlations are associated with specific, stimulus-dependent changes in the efficiency of the population code, and are consistent with changes in perceptual performance after adaptation. Our results have implications beyond the predictions of current theories of sensory coding, suggesting that brief adaptation improves the accuracy of population coding to optimize neuronal performance during natural viewing.

Assessment of stimulus-induced changes in human V1 visual field maps.

Visual cortex contains a set of field maps in which nearby scene points are represented in the responses of nearby neurons. We tested a recent hypothesis that the visual field map in primary visual cortex (V1) is dynamic, changing in response to stimulus motion direction. The original experimental report replicates, but further experimental and analytical investigations do not support, the interpretation of the results. The V1 map remains invariant when measured using stimuli moving in different directions. The measurements can be explained by small and systematic response amplitude differences that arise when probing with stimuli moving in different directions.

Contrast response in visual cortex: quantitative assessment with intrinsic optical signal imaging and neural firing.

While previous studies showed that intrinsic optical signals spatially correspond with electrophysiological responses in mammalian visual cortex, the quantitative correspondence of their response strengths is open to question. Measurement of both signals' strength as functions of visual stimulus contrast provides an opportunity for quantitative comparison. Towards that end, the spatial and temporal properties of the optical signal impose important constraints upon quantification of its strength. We used intrinsic optical signal imaging and single unit recording to measure responses to drifting gratings at contrasts ranging from 10-80% in cat area 18. We calculated the average difference images for pairs of oppositely moving, or orthogonally oriented, gratings at each contrast and evaluated three different methods for quantifying optical signal strength. After about 2.5 s, the spatial patterns of optical images and the time course of their strength were contrast-invariant. This "space-time-contrast separability" for optical response implies a spatial uniformity of the optical contrast response functions, provides an objective basis to guide temporal averaging of optical signals, and validates a scalar metric of optical signal strength. Optically measured contrast response functions increase monotonically and saturate at high contrasts, qualitatively resembling those from single units. However, quantitative comparison reveals a nonlinear relationship with neural firing, such that the optical response reaches half of its maximum when the neural response has reached only around 20% of its maximum. This relationship suggests that intrinsic optical signals are relatively more sensitive to weak signals than neural firing.

Economy of scale: a motion sensor with variable speed tuning.

We have previously presented a model of how neurons in the primate middle temporal (MT/V5) area can develop selectivity for image speed by using common properties of the V1 neurons that precede them in the visual motion pathway (J. A. Perrone & A. Thiele, 2002). The motion sensor developed in this model is based on two broad classes of V1 complex neurons (sustained and transient). The S-type neuron has low-pass temporal frequency tuning, p(omega), and the T-type has band-pass temporal frequency tuning, m(omega). The outputs from the S and T neurons are combined in a special way (weighted intersection mechanism [WIM]) to generate a sensor tuned to a particular speed, v. Here I go on to show that if the S and T temporal frequency tuning functions have a particular form (i.e., p(omega)/(m(omega) = k/omega), then a motion sensor with variable speed tuning can be generated from just two V1 neurons. A simple scaling of the S- or T-type neuron output before it is incorporated into the WIM model produces a motion sensor that can be tuned to a wide continuous range of optimal speeds.

Binocular disparity encoding cells generated through an Infomax based learning algorithm.

A learning algorithm for a model binocular cell was derived according to an information maximization principle and by using a low signal-to-noise-ratio approximation. The algorithm updates cell's synaptic weights so that the information obtained from the cell's output is increased. According to the algorithm, model binocular cells were trained by using computer-generated stereo images as training data. As a result, cells tuned to various disparities were generated. Also, generated synaptic weight patterns of the cells were similar to Gabor-wavelets and receptive fields of simple cells in the visual cortex. Thus, they were orientation and spatial frequency selective as well as disparity selective. Gabor functions were used to fit the generated weight patterns. The fitting results indicated that the generated cells encode disparities in terms of phase disparity and/or position disparity. This result agrees with experimental findings by Anzai et al. [J Neurophys 82 (1999) 874] and is consistent with ICA-based theoretical results obtained [Network: Comput Neural Syst 11 (2000) 191].

Attractor dynamics of network UP states in the neocortex.

The cerebral cortex receives input from lower brain regions, and its function is traditionally considered to be processing that input through successive stages to reach an appropriate output. However, the cortical circuit contains many interconnections, including those feeding back from higher centres, and is continuously active even in the absence of sensory inputs. Such spontaneous firing has a structure that reflects the coordinated activity of specific groups of neurons. Moreover, the membrane potential of cortical neurons fluctuates spontaneously between a resting (DOWN) and a depolarized (UP) state, which may also be coordinated. The elevated firing rate in the UP state follows sensory stimulation and provides a substrate for persistent activity, a network state that might mediate working memory. Using two-photon calcium imaging, we reconstructed the dynamics of spontaneous activity of up to 1,400 neurons in slices of mouse visual cortex. Here we report the occurrence of synchronized UP state transitions ('cortical flashes') that occur in spatially organized ensembles involving small numbers of neurons. Because of their stereotyped spatiotemporal dynamics, we conclude that network UP states are circuit attractors--emergent features of feedback neural networks that could implement memory states or solutions to computational problems.

Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps.

The axonal (bouton) distributions of a layer 4 clutch cell (CC), two layer 3 medium-sized basket cells (MBC), and a layer 3 large basket cell (LBC) to orientation, direction, and ocular dominance maps were studied quantitatively. 1) The CC provided exclusively local projections (<380 microm from the soma) and contacted a narrow "niche" of functional representations. 2) The two MBCs emitted local projections (75% and 79% of all boutons), which were engaged with isoorientations (61% and 48%) and isodirections, and long-range projections (25% and 21%, >313 microm and >418 microm), which encountered cross-orientation sites (14% and 12%) and isoorientation sites (7% and 5%). Their direction preferences were mainly perpendicular to or opposite those of local projections. 3) The LBC provided the majority (60%) of its boutons to long-range distances (>437 microm). Locally, LBC boutons showed a rather balanced contribution to isoorientations (19%) and cross-orientations (12%) and preferred isodirections. Remotely, however, cross-orientation sites were preferred (31% vs. 23%) and the directional output was balanced. 4) Monte Carlo simulations revealed that the differences between the orientation specificity of local and long-range projections cannot be explained by a homogeneous lateral distribution of the boutons. 5) There was a similar eye preference in the local and long-range projection fields of the MBCs. The LBC contacted both contra- and ipsilateral eye domains. 6) The basket axons showed little laminar difference in orientation and direction topography. The results suggest that an individual basket cell can mediate a wide range of effects depending on the size and termination pattern of the axonal field.

Uniformity, specificity and variability of corticocortical connectivity.

In many studies of the mammalian brain, subjective assessments of connectivity patterns and connection strengths have been used to subdivide the cortex into separate but linked areas and to make deductions about the flow of information through the cortical network. Here we describe the results of applying statistical analyses to quantitative corticocortical connection data, and the conclusions that can be drawn from such quantitative approaches. Injections of the tracer WGA-HRP were made into different visual areas either side of the middle suprasylvian sulcus (MSS) in 11 adult cats. Retrogradely labelled cells produced by these injections were counted in selected coronal sections taken at regularly spaced intervals (1 mm) through the entire visual cortex, and their cumulative sums and relative proportions in each of 16 recognized visual cortical areas were computed. The surface dimensions of these areas were measured in each cat, from contour lines made on enlarged drawings of the same sections. A total of 116,149 labelled neurons were assigned to all visual cortical areas in the 11 cats, with 5212 others excluded because of their uncertain location. The distribution of relative connection strengths, that is, the percentage of labelled cells per cortical area, was evaluated using non-parametric cluster analyses and Monte Carlo simulation, and relationships between connection strength and area size were examined by linear regression. The absolute size of each visual cortical area was uniform across individual cats, whereas the strengths of connections between the same area pairs were extremely variable for injections in different animals. The overall distribution of labelling strengths for corticocortical connections was continuous and monotonic, rather than inherently clustered, with the highest frequencies presented by the absent (zero density) and the very-low-density connections. These two categories could not, on analytical grounds, be separated from each other. Thus it seems that any subjective description of corticocortical connectivity strengths by ordinal classes (such as 'absent', 'weak', 'moderate' or 'strong') imposes a categorization on the data, rather than recognizes a structure inherent in the data themselves. Despite the great variability of connections, similarities in the distribution profiles for the relative strengths of labelled cells in all areas could be used to identify clusters of different injection sites in the MSS. This supported the conclusion that there are four connectionally distinct subdivisions of this cortex, corresponding to areas 21a, PMLS and AMLS (in the medial bank) and to area PLLS (in the lateral bank). Even for tracer deposits in the same cortical subdivision, however, the strength of connections projecting to the site from other cortical areas varied greatly across injection in different individual animals. We further demonstrated that, on average, the strength of connections originating from any given cortical area was positively and linearly correlated with the size of its surface dimensions. When analysed by specific injection site location, however, this relationship was shown to hold for the individual connections to the medial bank MSS areas, but not for connections leading to the lateral bank area. The data suggest that connectivity of the cat's visual cortex possesses a number of uniform global features, which are locally organized in such a way as to give each cortical area unique characteristics.

Attention modulates contextual influences in the primary visual cortex of alert monkeys.

The response properties of cells in the primary visual cortex (V1) were measured while the animals directed their attention either to the position of the neuron's receptive field (RF), to a position away from the RF (focal attention), or to four locations in the visual field (distributed attention). Over the population, varying attentional state had no significant effect on the response to an isolated stimulus within the RF but had a large influence on the facilitatory effects of contextual lines. We propose that the attentional modulation of contextual effects represents a gating of long range horizontal connections within area V1 by feedback connections to V1 and that this gating provides a mechanism for shaping responses under attention to stimulus configuration.

Vertical disparity, egocentric distance and stereoscopic depth constancy: a new interpretation.

There has long been a problem concerning the presence in the visual cortex of binocularly activated cells that are selective for vertical stimulus disparities because it is generally believed that only horizontal disparities contribute to stereoscopic depth perception. The accepted view is that stereoscopic depth estimates are only relative to the fixation point and that independent information from an extraretinal source is needed to scale for absolute or egocentric distance. Recently, however, theoretical computations have shown that egocentric distance can be estimated directly from vertical disparities without recourse to extraretinal sources. There has been little impetus to follow up these computations with experimental observations, because the vertical disparities that normally occur between the images in the two eyes have always been regarded as being too small to be of significance for visual perception and because experiments have consistently shown that our conscious appreciation of egocentric distance is rather crude and unreliable. Nevertheless, the veridicality of stereoscopic depth constancy indicates that accurate distance information is available to the visual system and that the information about egocentric distance and horizontal disparity are processed together so as to continually recalibrate the horizontal disparity values for different absolute distances. Computations show that the recalibration can be based directly on vertical disparities without the need for any intervening estimates of absolute distance. This may partly explain the relative crudity of our conscious appreciation of egocentric distance. From published data it has been possible to calculate the magnitude of the vertical disparities that the human visual system must be able to discriminate in order for depth constancy to have the observed level of veridicality. From published data on the induced effect it has also been possible to calculate the threshold values for the detection of vertical disparities by the visual system. These threshold values are smaller than those needed to provide for the recalibration of the horizontal disparities in the interests of veridical depth constancy. An outline is given of the known properties of the binocularly activated cells in the striate cortex that are able to discriminate and assess the vertical disparities. Experiments are proposed that should validate, or otherwise, the concepts put forward in this paper.

A simple statistical test for the vertex ratio using Monte Carlo simulation.

The vertex ratio is the crucial quantity in vertex analysis, which is a method to characterize the mode of growth of neuronal tree structures (i.e. dendrites and axons). In this report we propose the use of the Monte Carlo test to calculate a level of significance for the vertex ratio. As a result the vertex ratio can be used to analyse neuronal trees with respect to a range of growth hypotheses, including terminal and segmental growth.