Brief Stimuli Cast a Persistent Long-Term Trace in Visual Cortex.

Visual processing is strongly influenced by recent stimulus history, a phenomenon termed adaptation. Prominent theories cast adaptation as a consequence of optimized encoding of visual information by exploiting the temporal statistics of the world. However, this would require the visual system to track the history of individual briefly experienced events, within a stream of visual input, to build up statistical representations over longer timescales. Here, using an openly available dataset from the Allen Brain Observatory, we show that neurons in the early visual cortex of the mouse indeed maintain long-term traces of individual past stimuli that persist despite the presentation of several intervening stimuli, leading to long-term and stimulus-specific adaptation over dozens of seconds. Long-term adaptation was selectively expressed in cortical, but not in thalamic, neurons, which only showed short-term adaptation. Early visual cortex thus maintains concurrent stimulus-specific memory traces of past input, enabling the visual system to build up a statistical representation of the world to optimize the encoding of new information in a changing environment.SIGNIFICANCE STATEMENT In the natural world, previous sensory input is predictive of current input over multisecond timescales. The visual system could exploit these predictabilities by adapting current visual processing to the long-term history of visual input. However, it is unclear whether the visual system can track the history of individual briefly experienced images, within a stream of input, to build up statistical representations over such long timescales. Here, we show that neurons in early visual cortex of the mouse brain exhibit remarkably long-term adaptation to brief stimuli, persisting over dozens of seconds, and despite the presentation of several intervening stimuli. The visual cortex thus maintains long-term traces of individual briefly experienced past images, enabling the formation of statistical representations over extended timescales.

Fractal spike dynamics and neuronal coupling in the primate visual system.

KEY POINTS: We measured fractal (self-similar) fluctuations in ongoing spiking activity in subcortical (lateral geniculate nucleus, LGN) and cortical (area MT) visual areas in anaesthetised marmosets. Cells in the evolutionary ancient koniocellular LGN pathway and in area MT show high-amplitude fractal fluctuations, whereas evolutionarily newer parvocellular and magnocellular LGN cells do not. Spiking activity in koniocellular cells and MT cells shows substantial correlation to the local population activity, whereas activity in parvocellular and magnocellular cells is less correlated with local activity. We develop a model consisting of a fractal process and a global rate modulation which can reproduce and explain the fundamental relationship between fractal fluctuations and population coupling in LGN and MT. The model provides a unified account of apparently disparate aspects of neural spiking activity and can improve our understanding of information processing in evolutionary ancient and modern visual pathways. ABSTRACT: The brain represents and processes information through patterns of spiking activity, which is influenced by local and widescale brain circuits as well as intrinsic neural dynamics. Whether these influences have independent or linked effects on spiking activity is, however, not known. Here we measured spiking activity in two visual centres, the lateral geniculate nucleus (LGN) and cortical area MT, in marmoset monkeys. By combining the Fano-factor time curve, power spectral analysis and rescaled range analysis, we reveal inherent fractal fluctuations of spiking activity in LGN and MT. We found that the evolutionary ancient koniocellular (K) pathway in LGN and area MT exhibits strong fractal fluctuations at short (<1 s) time scales. Parvocellular (P) and magnocellular (M) LGN cells show weaker fractal fluctuations at longer (multi-second) time scales. In both LGN and MT, the amplitude and time scale of fractal fluctuations can explain short and long time scale spiking dynamics. We further show differential neuronal coupling of LGN and MT cells to local population spiking activity. The population coupling is intrinsically linked to fractal fluctuations: neurons showing stronger fluctuations are more strongly correlated to the local population activity. To understand this relationship, we modelled spiking activity using a fractal inhomogeneous Poisson process with dynamic rate, which is the product of an intrinsic stochastic fractal rate and a global modulatory gain. Our model explains the intrinsic links between neuronal spike rate and population coupling in LGN and MT, and establishes a unified account of dynamic spiking properties in afferent visual pathways.

Temporal Contingencies Determine Whether Adaptation Strengthens or Weakens Normalization.

A fundamental and nearly ubiquitous feature of sensory encoding is that neuronal responses are strongly influenced by recent experience, or adaptation. Theoretical and computational studies have proposed that many adaptation effects may result in part from changes in the strength of normalization signals. Normalization is a "canonical" computation in which a neuron's response is modulated (normalized) by the pooled activity of other neurons. Here, we test whether adaptation can alter the strength of cross-orientation suppression, or masking, a paradigmatic form of normalization evident in primary visual cortex (V1). We made extracellular recordings of V1 neurons in anesthetized male macaques and measured responses to plaid stimuli composed of two overlapping, orthogonal gratings before and after prolonged exposure to two distinct adapters. The first adapter was a plaid consisting of orthogonal gratings and led to stronger masking. The second adapter presented the same orthogonal gratings in an interleaved manner and led to weaker masking. The strength of adaptation's effects on masking depended on the orientation of the test stimuli relative to the orientation of the adapters, but was independent of neuronal orientation preference. Changes in masking could not be explained by altered neuronal responsivity. Our results suggest that normalization signals can be strengthened or weakened by adaptation depending on the temporal contingencies of the adapting stimuli. Our findings reveal an interplay between two widespread computations in cortical circuits, adaptation and normalization, that enables flexible adjustments to the structure of the environment, including the temporal relationships among sensory stimuli.SIGNIFICANCE STATEMENT Two fundamental features of sensory responses are that they are influenced by adaptation and that they are modulated by the activity of other nearby neurons via normalization. Our findings reveal a strong interaction between these two aspects of cortical computation. Specifically, we show that cross-orientation masking, a form of normalization, can be strengthened or weakened by adaptation depending on the temporal contingencies between sensory inputs. Our findings support theoretical proposals that some adaptation effects may involve altered normalization and offer a network-based explanation for how cortex adjusts to current sensory demands.

Receptive Field Properties of Koniocellular On/Off Neurons in the Lateral Geniculate Nucleus of Marmoset Monkeys.

The koniocellular (K) layers of the primate dorsal lateral geniculate nucleus house a variety of visual receptive field types, not all of which have been fully characterized. Here we made single-cell recordings targeted to the K layers of diurnal New World monkeys (marmosets). A subset of recorded cells was excited by both increments and decrements of light intensity (on/off-cells). Histological reconstruction of the location of these cells confirmed that they are segregated to K layers; we therefore refer to these cells as K-on/off cells. The K-on/off cells show high contrast sensitivity, strong bandpass spatial frequency tuning, and their response magnitude is strongly reduced by stimuli larger than the excitatory receptive field (silent suppressive surrounds). Stationary counterphase gratings evoke unmodulated spike rate increases or frequency-doubled responses in K-on/off cells; such responses are largely independent of grating spatial phase. The K-on/off cells are not orientation or direction selective. Some (but not all) properties of K-on/off cells are consistent with those of local-edge-detector/impressed-by-contrast cells reported in studies of cat retina and geniculate, and broad-thorny ganglion cells recorded in macaque monkey retina. The receptive field properties of K-on/off cells and their preferential location in the ventral K layers (K1 and K2) make them good candidates for the direct projection from geniculate to extrastriate cortical area MT/V5. If so, they could contribute to visual information processing in the dorsal ("where" or "action") visual stream.SIGNIFICANCE STATEMENT We characterize cells in an evolutionary ancient part of the visual pathway in primates. The cells are located in the lateral geniculate nucleus (the main visual afferent relay nucleus), in regions called koniocellular layers that are known to project to extrastriate visual areas as well as primary visual cortex. The cells show high contrast sensitivity and rapid, transient responses to light onset and offset. Their properties suggest they could contribute to visual processing in the dorsal ("where" or "action") visual stream.

Visual Motion Discrimination by Propagating Patterns in Primate Cerebral Cortex.

Visual stimuli can evoke waves of neural activity that propagate across the surface of visual cortical areas. The relevance of these waves for visual processing is unknown. Here, we measured the phase and amplitude of local field potentials (LFPs) in electrode array recordings from the motion-processing medial temporal (MT) area of anesthetized male marmosets. Animals viewed grating or dot-field stimuli drifting in different directions. We found that, on individual trials, the direction of LFP wave propagation is sensitive to the direction of stimulus motion. Propagating LFP patterns are also detectable in trial-averaged activity, but the trial-averaged patterns exhibit different dynamics and behaviors from those in single trials and are similar across motion directions. We show that this difference arises because stimulus-sensitive propagating patterns are present in the phase of single-trial oscillations, whereas the trial-averaged signal is dominated by additive amplitude effects. Our results demonstrate that propagating LFP patterns can represent sensory inputs at timescales relevant to visually guided behaviors and raise the possibility that propagating activity patterns serve neural information processing in area MT and other cortical areas.SIGNIFICANCE STATEMENT Propagating wave patterns are widely observed in the cortex, but their functional relevance remains unknown. We show here that visual stimuli generate propagating wave patterns in local field potentials (LFPs) in a movement-sensitive area of the primate cortex and that the propagation direction of these patterns is sensitive to stimulus motion direction. We also show that averaging LFP signals across multiple stimulus presentations (trial averaging) yields propagating patterns that capture different dynamic properties of the LFP response and show negligible direction sensitivity. Our results demonstrate that sensory stimuli can modulate propagating wave patterns reliably in the cortex. The relevant dynamics are normally masked by trial averaging, which is a conventional step in LFP signal processing.

Visual response properties of neurons in the superficial layers of the superior colliculus of awake mouse.

KEY POINTS: In rodents, including mice, the superior colliculus is the major target of the retina, but its visual response is not well characterized. In the present study, extracellular recordings from single nerve cells in the superficial layers of the superior colliculus were made in awake, head-restrained mice, and their responses to visual stimuli were measured. It was found that these neurons show brisk, highly sensitive and short latency visual responses, a preference for black over white stimuli, and diverse responses to moving patterns. At least five broad classes can be defined by variation in functional properties among units. The results of the present study demonstrate that eye movements have a measurable impact on visual responses in awake animals and show how they may be mitigated in analyses. ABSTRACT: The mouse is an increasingly important animal model of visual function in health and disease. In mice, most retinal signals are routed through the superficial layers of the midbrain superior colliculus, and it is well established that much of the visual behaviour of mice relies on activity in the superior colliculus. The functional organization of visual signals in the mouse superior colliculus is, however, not well established in awake animals. We therefore made extracellular recordings from the superficial layers of the superior colliculus in awake mice, while the animals were viewing visual stimuli including flashed spots and drifting gratings. We find that neurons in the superficial layers of the superior colliculus of awake mouse generally show short latency, brisk responses. Receptive fields are usually 'ON-OFF' with a preference for black stimuli, and are weakly non-linear in response to gratings and other forms of luminance modulation. Population responses to drifting gratings are highly contrast sensitive, with a robust response to spatial frequencies above 0.3 cycles degree-1 and temporal frequencies above 15 Hz. The receptive fields are also often speed-tuned or direction-selective. Analysis of the response across multiple stimulus dimensions reveals at least five functionally distinct groups of units. We also find that eye movements affect measurements of receptive field properties in awake animals, and show how these may be mitigated in analyses. Qualitatively similar responses were obtained in urethane-anaesthetized animals, although receptive fields in awake animals had higher contrast sensitivity, shorter visual latency and a stronger response to high temporal frequencies.

Interpreting the dimensions of neural feature representations revealed by dimensionality reduction.

Recent progress in understanding the structure of neural representations in the cerebral cortex has centred around the application of multivariate classification analyses to measurements of brain activity. These analyses have proved a sensitive test of whether given brain regions provide information about specific perceptual or cognitive processes. An exciting extension of this approach is to infer the structure of this information, thereby drawing conclusions about the underlying neural representational space. These approaches rely on exploratory data-driven dimensionality reduction to extract the natural dimensions of neural spaces, including natural visual object and scene representations, semantic and conceptual knowledge, and working memory. However, the efficacy of these exploratory methods is unknown, because they have only been applied to representations in brain areas for which we have little or no secondary knowledge. One of the best-understood areas of the cerebral cortex is area MT of primate visual cortex, which is known to be important in motion analysis. To assess the effectiveness of dimensionality reduction for recovering neural representational space we applied several dimensionality reduction methods to multielectrode measurements of spiking activity obtained from area MT of marmoset monkeys, made while systematically varying the motion direction and speed of moving stimuli. Despite robust tuning at individual electrodes, and high classifier performance, dimensionality reduction rarely revealed dimensions for direction and speed. We use this example to illustrate important limitations of these analyses, and suggest a framework for how to best apply such methods to data where the structure of the neural representation is unknown.

Spectral Signatures of Feedforward and Recurrent Circuitry in Monkey Area MT.

Recordings of local field potential (LFP) in the visual cortex can show rhythmic activity at gamma frequencies (30-100 Hz). While the gamma rhythms in the primary visual cortex have been well studied, the structural and functional characteristics of gamma rhythms in extrastriate visual cortex are less clear. Here, we studied the spatial distribution and functional specificity of gamma rhythms in extrastriate middle temporal (MT) area of visual cortex in marmoset monkeys. We found that moving gratings induced narrowband gamma rhythms across cortical layers that were coherent across much of area MT. Moving dot fields instead induced a broadband increase in LFP in middle and upper layers, with weaker narrowband gamma rhythms in deeper layers. The stimulus dependence of LFP response in middle and upper layers of area MT appears to reflect the presence (gratings) or absence (dot fields and other textures) of strongly oriented contours. Our results suggest that gamma rhythms in these layers are propagated from earlier visual cortex, while those in the deeper layers may emerge in area MT.

Relationship between cortical state and spiking activity in the lateral geniculate nucleus of marmosets.

KEY POINTS: How parallel are the primate visual pathways? In the present study, we demonstrate that parallel visual pathways in the dorsal lateral geniculate nucleus (LGN) show distinct patterns of interaction with rhythmic activity in the primary visual cortex (V1). In the V1 of anaesthetized marmosets, the EEG frequency spectrum undergoes transient changes that are characterized by fluctuations in delta-band EEG power. We show that, on multisecond timescales, spiking activity in an evolutionary primitive (koniocellular) LGN pathway is specifically linked to these slow EEG spectrum changes. By contrast, on subsecond (delta frequency) timescales, cortical oscillations can entrain spiking activity throughout the entire LGN. Our results are consistent with the hypothesis that, in waking animals, the koniocellular pathway selectively participates in brain circuits controlling vigilance and attention. ABSTRACT: The major afferent cortical pathway in the visual system passes through the dorsal lateral geniculate nucleus (LGN), where nerve signals originating in the eye can first interact with brain circuits regulating visual processing, vigilance and attention. In the present study, we investigated how ongoing and visually driven activity in magnocellular (M), parvocellular (P) and koniocellular (K) layers of the LGN are related to cortical state. We recorded extracellular spiking activity in the LGN simultaneously with local field potentials (LFP) in primary visual cortex, in sufentanil-anaesthetized marmoset monkeys. We found that asynchronous cortical states (marked by low power in delta-band LFPs) are linked to high spike rates in K cells (but not P cells or M cells), on multisecond timescales. Cortical asynchrony precedes the increases in K cell spike rates by 1-3 s, implying causality. At subsecond timescales, the spiking activity in many cells of all (M, P and K) classes is phase-locked to delta waves in the cortical LFP, and more cells are phase-locked during synchronous cortical states than during asynchronous cortical states. The switch from low-to-high spike rates in K cells does not degrade their visual signalling capacity. By contrast, during asynchronous cortical states, the fidelity of visual signals transmitted by K cells is improved, probably because K cell responses become less rectified. Overall, the data show that slow fluctuations in cortical state are selectively linked to K pathway spiking activity, whereas delta-frequency cortical oscillations entrain spiking activity throughout the entire LGN, in anaesthetized marmosets.

Dynamic population codes of multiplexed stimulus features in primate area MT.

The middle-temporal area (MT) of primate visual cortex is critical in the analysis of visual motion. Single-unit studies suggest that the response dynamics of neurons within area MT depend on stimulus features, but how these dynamics emerge at the population level, and how feature representations interact, is not clear. Here, we used multivariate classification analysis to study how stimulus features are represented in the spiking activity of populations of neurons in area MT of marmoset monkey. Using representational similarity analysis we distinguished the emerging representations of moving grating and dot field stimuli. We show that representations of stimulus orientation, spatial frequency, and speed are evident near the onset of the population response, while the representation of stimulus direction is slower to emerge and sustained throughout the stimulus-evoked response. We further found a spatiotemporal asymmetry in the emergence of direction representations. Representations for high spatial frequencies and low temporal frequencies are initially orientation dependent, while those for high temporal frequencies and low spatial frequencies are more sensitive to motion direction. Our analyses reveal a complex interplay of feature representations in area MT population response that may explain the stimulus-dependent dynamics of motion vision.NEW & NOTEWORTHY Simultaneous multielectrode recordings can measure population-level codes that previously were only inferred from single-electrode recordings. However, many multielectrode recordings are analyzed using univariate single-electrode analysis approaches, which fail to fully utilize the population-level information. Here, we overcome these limitations by applying multivariate pattern classification analysis and representational similarity analysis to large-scale recordings from middle-temporal area (MT) in marmoset monkeys. Our analyses reveal a dynamic interplay of feature representations in area MT population response.

Emergence of complex wave patterns in primate cerebral cortex.

Slow brain rhythms are attributed to near-simultaneous (synchronous) changes in activity in neuron populations in the brain. Because they are slow and widespread, synchronous rhythms have not been considered crucial for information processing in the waking state. Here we adapted methods from turbulence physics to analyze δ-band (1-4 Hz) rhythms in local field potential (LFP) activity, in multielectrode recordings from cerebral cortex in anesthetized marmoset monkeys. We found that synchrony contributes only a small fraction (less than one-fourth) to the local spatiotemporal structure of δ-band signals. Rather, δ-band activity is dominated by propagating plane waves and spatiotemporal structures, which we call complex waves. Complex waves are manifest at submillimeter spatial scales, and millisecond-range temporal scales. We show that complex waves can be characterized by their relation to phase singularities within local nerve cell networks. We validate the biological relevance of complex waves by showing that nerve cell spike rates are higher in presence of complex waves than in the presence of synchrony and that there are nonrandom patterns of evolution from one type of complex wave to another. We conclude that slow brain rhythms predominantly indicate spatiotemporally organized activity in local nerve cell circuits, not synchronous activity within and across brain regions.

fMRI mapping of the visual system in the mouse brain with interleaved snapshot GE-EPI.

The use of functional magnetic resonance imaging (fMRI) in mice is increasingly prevalent, providing a means to non-invasively characterise functional abnormalities associated with genetic models of human diseases. The predominant stimulus used in task-based fMRI in the mouse is electrical stimulation of the paw. Task-based fMRI in mice using visual stimuli remains underexplored, despite visual stimuli being common in human fMRI studies. In this study, we map the mouse brain visual system with BOLD measurements at 9.4T using flashing light stimuli with medetomidine anaesthesia. BOLD responses were observed in the lateral geniculate nucleus, the superior colliculus and the primary visual area of the cortex, and were modulated by the flashing frequency, diffuse vs focussed light and stimulus context. Negative BOLD responses were measured in the visual cortex at 10Hz flashing frequency; but turned positive below 5Hz. In addition, the use of interleaved snapshot GE-EPI improved fMRI image quality without diminishing the temporal contrast-noise-ratio. Taken together, this work demonstrates a novel methodological protocol in which the mouse brain visual system can be non-invasively investigated using BOLD fMRI.

Local and Global Correlations between Neurons in the Middle Temporal Area of Primate Visual Cortex.

In humans and other primates, the analysis of visual motion includes populations of neurons in the middle-temporal (MT) area of visual cortex. Motion analysis will be constrained by the structure of neural correlations in these populations. Here, we use multi-electrode arrays to measure correlations in anesthetized marmoset, a New World monkey where area MT lies exposed on the cortical surface. We measured correlations in the spike count between pairs of neurons and within populations of neurons, for moving dot fields and moving gratings. Correlations were weaker in area MT than in area V1. The magnitude of correlations in area MT diminished with distance between receptive fields, and difference in preferred direction. Correlations during presentation of moving gratings were stronger than those during presentation of moving dot fields, extended further across cortex, and were less dependent on the functional properties of neurons. Analysis of the timescales of correlation suggests presence of 2 mechanisms. A local mechanism, associated with near-synchronous spiking activity, is strongest in nearby neurons with similar direction preference and is independent of visual stimulus. A global mechanism, operating over larger spatial scales and longer timescales, is independent of direction preference and is modulated by the type of visual stimulus presented.

Spatial precision of population activity in primate area MT.

The middle temporal (MT) area is a cortical area integral to the "where" pathway of primate visual processing, signaling the movement and position of objects in the visual world. The receptive field of a single MT neuron is sensitive to the direction of object motion but is too large to signal precise spatial position. Here, we asked if the activity of MT neurons could be combined to support the high spatial precision required in the where pathway. With the use of multielectrode arrays, we recorded simultaneously neural activity at 24-65 sites in area MT of anesthetized marmoset monkeys. We found that although individual receptive fields span more than 5° of the visual field, the combined population response can support fine spatial discriminations (<0.2°). This is because receptive fields at neighboring sites overlapped substantially, and changes in spatial position are therefore projected onto neural activity in a large ensemble of neurons. This fine spatial discrimination is supported primarily by neurons with receptive fields flanking the target locations. Population performance is degraded (by 13-22%) when correlations in neural activity are ignored, further reflecting the contribution of population neural interactions. Our results show that population signals can provide high spatial precision despite large receptive fields, allowing area MT to represent both the motion and the position of objects in the visual world.

Multimodal optogenetic neural interfacing device fabricated by scalable optical fiber drawing technique.

We present a novel approach to the design and manufacture of optrodes for use in the biomedical research field of optogenetic neural interfacing. Using recently developed optical fiber drawing techniques that involve co-drawing metal/polymer composite fiber, we have assembled and characterized a novel optrode with promising optical and electrical functionality. The fabrication technique is flexible, scalable, and amenable to extension to implantable optrodes with high-density arrays of multiple electrodes, waveguides, and drug delivery channels.

Cortical-like receptive fields in the lateral geniculate nucleus of marmoset monkeys.

Most neurons in primary visual cortex (V1) exhibit high selectivity for the orientation of visual stimuli. In contrast, neurons in the main thalamic input to V1, the lateral geniculate nucleus (LGN), are considered to be only weakly orientation selective. Here we characterize a sparse population of cells in marmoset LGN that show orientation and spatial frequency selectivity as great as that of cells in V1. The recording position in LGN and histological reconstruction of these cells shows that they are part of the koniocellular (K) pathways. Accordingly we have named them K-o ("koniocellular-orientation") cells. Most K-o cells prefer vertically oriented gratings; their contrast sensitivity and TF tuning are similar to those of parvocellular cells, and they receive negligible functional input from short wavelength-sensitive ("blue") cone photoreceptors. Four K-o cells tested displayed binocular responses. Our results provide further evidence that in primates as in nonprimate mammals the cortical input streams include a diversity of visual representations. The presence of K-o cells increases functional homologies between K pathways in primates and "sluggish/W" pathways in nonprimate visual systems.

Integration and segregation of multiple motion signals by neurons in area MT of primate.

We used multielectrode arrays to measure the response of populations of neurons in primate middle temporal area to the transparent motion of two superimposed dot fields moving in different directions. The shape of the population response was well predicted by the sum of the responses to the constituent fields. However, the population response profile for transparent dot fields was similar to that for coherent plaid motion and hence an unreliable cue to transparency. We then used single-unit recording to characterize component and pattern cells from their response to drifting plaids. Unlike for plaids, component cells responded to the average direction of superimposed dot fields, whereas pattern cells could signal the constituent motions. This observation provides support for a strong prediction of the Simoncelli and Heeger (1998) model of motion analysis in area middle temporal, and suggests that pattern cells have a special status in the processing of superimposed dot fields.

Slow intrinsic rhythm in the koniocellular visual pathway.

Slow rhythmic changes in nerve-cell activity are characteristic of unconscious brain states and also may contribute to waking brain function by coordinating activity between cortical and subcortical structures. Here we show that slow rhythms are exhibited by the koniocellular (K) pathway, one of three visual pathways beginning in the eye and projecting through the lateral geniculate visual relay nucleus to the cerebral cortex. We recorded activity in pairs and ensembles of neurons in the lateral geniculate nucleus of anesthetized marmoset monkeys. We found slow rhythms are common in K cells but are rare in parvocellular and magnocellular cell pairs. The time course of slow K rhythms corresponds to subbeta (<10 Hz) EEG frequencies, and high spike rates in K cells are associated with low power in the theta and delta EEG bands. By contrast, spontaneous activity in the parvocellular and magnocellular pathways is neither synchronized nor strongly linked to EEG state. These observations suggest that parallel visual pathways not only carry different kinds of visual signals but also contribute differentially to brain circuits at the first synapse in the thalamus. Differential contribution of sensory streams to rhythmic brain circuits also raises the possibility that sensory stimuli can be tailored to modify brain rhythms.

Texture-dependent motion signals in primate middle temporal area.

Neurons in the middle temporal (MT) area of primate cortex provide an important stage in the analysis of visual motion. For simple stimuli such as bars and plaids some neurons in area MT--pattern cells--seem to signal motion independent of contour orientation, but many neurons--component cells--do not. Why area MT supports both types of receptive field is unclear. To address this we made extracellular recordings from single units in area MT of anaesthetised marmoset monkeys and examined responses to two-dimensional images with a large range of orientations and spatial frequencies. Component and pattern cell response remained distinct during presentation of these complex spatial textures. Direction tuning curves were sharpest in component cells when a texture contained a narrow range of orientations, but were similar across all neurons for textures containing all orientations. Response magnitude of pattern cells, but not component cells, increased with the spatial bandwidth of the texture. In addition, response variability in all neurons was reduced when the stimulus was rich in spatial texture. Fisher information analysis showed that component cells provide more informative responses than pattern cells when a texture contains a narrow range of orientations, but pattern cells had more informative responses for broadband textures. Component cells and pattern cells may therefore coexist because they provide complementary and parallel motion signals.

Excitatory and inhibitory contributions to receptive fields of alpha-like retinal ganglion cells in mouse.

The ON and OFF pathways that emerge at the first synapse in the retina are generally thought to be streamed in parallel to higher visual areas, but recent work shows cross talk at the level of retinal ganglion cells. The ON pathway drives inhibitory inputs onto some OFF ganglion cells, such that these neurons show "push-pull" convergence of OFF-excitation and ON-disinhibition. In this study we measure the spatial receptive field of excitatory and inhibitory inputs to OFF-sustained (OFF-S) retinal ganglion cells of mouse, establish how contrast adaptation modulates excitatory and inhibitory synaptic inputs, and show the pharmacology of the inhibitory inputs. We find that the spatial tuning properties of excitatory and inhibitory inputs are sufficient to determine the spatial profile of the spike output and that high spatial acuity may be particularly reliant on disinhibitory circuits. Contrast adaptation reduced excitation to OFF-S ganglion cells, as expected, and also unmasked an asymmetry in inhibitory inputs: disinhibition at light-off was immune to contrast adaptation, but inhibition at light-on was substantially reduced. In pharmacological experiments we confirm that inhibitory inputs are partly mediated by glycine, but our measurements also suggest a substantial role for GABA. Our observations therefore reveal functional diversity in the inhibitory inputs to OFF ganglion cells and suggest that in addition to enhancing operational range these inputs help shape the spatial receptive fields of ganglion cells.