This study demonstrates the functional importance of the Surround context relayed laterally in V1 by the horizontal connectivity, in controlling the latency and the gain of the cortical response to ...the feedforward visual drive. We report here four main findings: 1) a centripetal apparent motion sequence results in a shortening of the spiking latency of V1 cells, when the orientation of the local inducer and the global motion axis are both co-aligned with the RF orientation preference; 2) this contextual effects grows with visual flow speed, peaking at 150–250°/s when it matches the propagation speed of horizontal connectivity (0.15–0.25 mm/ms); 3) For this speed range, the axial sensitivity of V1 cells is tilted by 90° to become co-aligned with the orientation preference axis; 4) the strength of modulation by the surround context correlates with the spatiotemporal coherence of the apparent motion flow. Our results suggest an internally-generated binding process, linking local (orientation /position) and global (motion/direction) features as early as V1. This long-range diffusion process constitutes a plausible substrate in V1 of the human psychophysical bias in speed estimation for collinear motion. Since it is demonstrated in the anesthetized cat, this novel form of contextual control of the cortical gain and phase is a built-in property in V1, whose expression does not require behavioral attention and top-down control from higher cortical areas. We propose that horizontal connectivity participates in the propagation of an internal “prediction” wave, shaped by visual experience, which links contour co-alignment and global axial motion at an apparent speed in the range of saccade-like eye movements.
Synaptic noise is thought to be a limiting factor for computational efficiency in the brain. In visual cortex (V1), ongoing activity is present in vivo, and spiking responses to simple stimuli are ...highly unreliable across trials. Stimulus statistics used to plot receptive fields, however, are quite different from those experienced during natural visuomotor exploration. We recorded V1 neurons intracellularly in the anaesthetized and paralyzed cat and compared their spiking and synaptic responses to full field natural images animated by simulated eye-movements to those evoked by simpler (grating) or higher dimensionality statistics (dense noise). In most cells, natural scene animation was the only condition where high temporal precision (in the 10-20 ms range) was maintained during sparse and reliable activity. At the subthreshold level, irregular but highly reproducible membrane potential dynamics were observed, even during long (several 100 ms) "spike-less" periods. We showed that both the spatial structure of natural scenes and the temporal dynamics of eye-movements increase the signal-to-noise ratio by a non-linear amplification of the signal combined with a reduction of the subthreshold contextual noise. These data support the view that the sparsening and the time precision of the neural code in V1 may depend primarily on three factors: (1) broadband input spectrum: the bandwidth must be rich enough for recruiting optimally the diversity of spatial and time constants during recurrent processing; (2) tight temporal interplay of excitation and inhibition: conductance measurements demonstrate that natural scene statistics narrow selectively the duration of the spiking opportunity window during which the balance between excitation and inhibition changes transiently and reversibly; (3) signal energy in the lower frequency band: a minimal level of power is needed below 10 Hz to reach consistently the spiking threshold, a situation rarely reached with visual dense noise.
Spike timing-dependent plasticity (STDP) is considered as an ubiquitous rule for associative plasticity in cortical networks in vitro. However, limited supporting evidence for its functional role has ...been provided in vivo. In particular, there are very few studies demonstrating the co-occurrence of synaptic efficiency changes and alteration of sensory responses in adult cortex during Hebbian or STDP protocols. We addressed this issue by reviewing and comparing the functional effects of two types of cellular conditioning in cat visual cortex. The first one, referred to as the "covariance" protocol, obeys a generalized Hebbian framework, by imposing, for different stimuli, supervised positive and negative changes in covariance between postsynaptic and presynaptic activity rates. The second protocol, based on intracellular recordings, replicated in vivo variants of the theta-burst paradigm (TBS), proven successful in inducing long-term potentiation in vitro. Since it was shown to impose a precise correlation delay between the electrically activated thalamic input and the TBS-induced postsynaptic spike, this protocol can be seen as a probe of causal ("pre-before-post") STDP. By choosing a thalamic region where the visual field representation was in retinotopic overlap with the intracellularly recorded cortical receptive field as the afferent site for supervised electrical stimulation, this protocol allowed to look for possible correlates between STDP and functional reorganization of the conditioned cortical receptive field. The rate-based "covariance protocol" induced significant and large amplitude changes in receptive field properties, in both kitten and adult V1 cortex. The TBS STDP-like protocol produced in the adult significant changes in the synaptic gain of the electrically activated thalamic pathway, but the statistical significance of the functional correlates was detectable mostly at the population level. Comparison of our observations with the literature leads us to re-examine the experimental status of spike timing-dependent potentiation in adult cortex. We propose the existence of a correlation-based threshold in vivo, limiting the expression of STDP-induced changes outside the critical period, and which accounts for the stability of synaptic weights during sensory cortical processing in the absence of attention or reward-gated supervision.
Receptive fields in primary visual cortex (V1) are categorized as simple or complex, depending on their spatial selectivity to stimulus contrast polarity. We studied the dependence of this ...classification on visual context by comparing, in the same cell, the synaptic responses to three classical receptive field mapping protocols: sparse noise, ternary dense noise and flashed Gabor noise. Intracellular recordings revealed that the relative weights of simple-like and complex-like receptive field components were scaled so as to make the same receptive field more simple-like with dense noise stimulation and more complex-like with sparse or Gabor noise stimulations. However, once these context-dependent receptive fields were convolved with the corresponding stimulus, the balance between simple-like and complex-like contributions to the synaptic responses appeared to be invariant across input statistics. This normalization of the linear/nonlinear input ratio suggests a previously unknown form of homeostatic control of V1 functional properties, optimizing the network nonlinearities to the statistical structure of the visual input.
Synaptic Correlates of Low-Level Perception in V1 Gerard-Mercier, Florian; Carelli, Pedro V; Pananceau, Marc ...
The Journal of neuroscience,
2016-Apr-06, 2016-04-06, 20160406, Volume:
36, Issue:
14
Journal Article
Peer reviewed
Open access
The computational role of primary visual cortex (V1) in low-level perception remains largely debated. A dominant view assumes the prevalence of higher cortical areas and top-down processes in binding ...information across the visual field. Here, we investigated the role of long-distance intracortical connections in form and motion processing by measuring, with intracellular recordings, their synaptic impact on neurons in area 17 (V1) of the anesthetized cat. By systematically mapping synaptic responses to stimuli presented in the nonspiking surround of V1 receptive fields, we provide the first quantitative characterization of the lateral functional connectivity kernel of V1 neurons. Our results revealed at the population level two structural-functional biases in the synaptic integration and dynamic association properties of V1 neurons. First, subthreshold responses to oriented stimuli flashed in isolation in the nonspiking surround exhibited a geometric organization around the preferred orientation axis mirroring the psychophysical "association field" for collinear contour perception. Second, apparent motion stimuli, for which horizontal and feedforward synaptic inputs summed in-phase, evoked dominantly facilitatory nonlinear interactions, specifically during centripetal collinear activation along the preferred orientation axis, at saccadic-like speeds. This spatiotemporal integration property, which could constitute the neural correlate of a human perceptual bias in speed detection, suggests that local (orientation) and global (motion) information is already linked within V1. We propose the existence of a "dynamic association field" in V1 neurons, whose spatial extent and anisotropy are transiently updated and reshaped as a function of changes in the retinal flow statistics imposed during natural oculomotor exploration.
The computational role of primary visual cortex in low-level perception remains debated. The expression of this "pop-out" perception is often assumed to require attention-related processes, such as top-down feedback from higher cortical areas. Using intracellular techniques in the anesthetized cat and novel analysis methods, we reveal unexpected structural-functional biases in the synaptic integration and dynamic association properties of V1 neurons. These structural-functional biases provide a substrate, within V1, for contour detection and, more unexpectedly, global motion flow sensitivity at saccadic speed, even in the absence of attentional processes. We argue for the concept of a "dynamic association field" in V1 neurons, whose spatial extent and anisotropy changes with retinal flow statistics, and more generally for a renewed focus on intracortical computation.
In vivo intracellular electrophysiology offers the unique possibility of listening to the "synaptic rumor " of the cortical network, captured by a recording electrode in a single V1 cell. It allows ...one to reconstruct the distribution of input sources in space and time, i.e. the effective network dynamics. We have used a reverse engineering method to demonstrate the propagation of visually evoked activity through lateral (and feedback) connectivity in the primary cortex of higher mammals. This approach, based on synaptic echography, is compared here with a real-time brain imaging technique based on voltage-sensitive dye imaging. The former method gives access to the microscopic convergence processes of single neurons, whereas the latter describes the macroscopic divergence process on the neuronal map. A combination of the two techniques can be used to elucidate the cortical origin of low-level (non attentive) binding processes participating in the emergence of Gestalt percepts.
In classic conditioning, the interstimulus interval (ISI) between the conditioned (CS) and unconditioned (US) stimulus is a critical parameter. The aim of the present experiment was to assess ...whether, during conditioning, modification of the CS-US interval could reliably produce changes in the functional properties of the interposito-thalamo-cortical pathways (INTCps). Five cats were prepared for chronic stimulation and recording from several brain regions along this pathway in awake animals. The CS was a weak electric shock applied on the interposed nucleus of the cerebellum in sites that initially elicited forelimb flexion (i.e., alpha motor responses) in three cats, and equal proportions of flexor and extensor responses in two cats. The US was an electric shock applied on the skin that elicited forelimb flexions. The motor and neurobiological effects of synchronous CS-US were compared with pairings in which the CS was applied 100 ms before US. Simultaneous and sequential application of CS and US produced different behavioral outcomes and resulted in different neural processes in the interposito-thalamo-cortical pathways (INTCps). The simultaneous presentation of stimuli only produced a small increase in excitability spreading to all the body representational zones of the primary motor cortex and a weak increase in the amplitude of the alpha motor response. In contrast, the sequential application led to a profound modification of the interposed output to neurons in the forelimb representation of the motor cortex. These robust neuronal correlates of conditioning were accompanied by a large facilitation of the alpha motor response (alpha-MR). There were also changes in the direction of misdirected alpha responses and an emergence of functionally appropriate, long-latency withdrawal forelimb flexion. These data revealed that, during conditioning, plastic changes within the thalamocortical connections are selectively induced by sequential information from central and peripheral afferents. This sequence significantly contributed to neural processes that are responsible for the acquisition, expression, and extinction of anticipatory flexion responses.
An examination of how widely distributed and specialized activities of the brain are flexibly and effectively coordinated.
A fundamental shift is occurring in neuroscience and related disciplines. In ...the past, researchers focused on functional specialization of the brain, discovering complex processing strategies based on convergence and divergence in slowly adapting anatomical architectures. Yet for the brain to cope with ever-changing and unpredictable circumstances, it needs strategies with richer interactive short-term dynamics. Recent research has revealed ways in which the brain effectively coordinates widely distributed and specialized activities to meet the needs of the moment. This book explores these findings, examining the functions, mechanisms, and manifestations of distributed dynamical coordination in the brain and mind across different species and levels of organization. The book identifies three basic functions of dynamic coordination: contextual disambiguation, dynamic grouping, and dynamic routing. It considers the role of dynamic coordination in temporally structured activity and explores these issues at different levels, from synaptic and local circuit mechanisms to macroscopic system dynamics, emphasizing their importance for cognition, behavior, and psychopathology.
Contributors
Evan Balaban, György Buzsáki, Nicola S. Clayton, Maurizio Corbetta, Robert Desimone, Kamran Diba, Shimon Edelman, Andreas K. Engel, Yves Fregnac, Pascal Fries, Karl Friston, Ann Graybiel, Sten Grillner, Uri Grodzinski, John-Dylan Haynes, Laurent Itti, Erich D. Jarvis, Jon H. Kaas, J.A. Scott Kelso, Peter König, Nancy J. Kopell, Ilona Kovács, Andreas Kreiter, Anders Lansner, Gilles Laurent, Jörg Lücke, Mikael Lundqvist, Angus MacDonald, Kevan Martin, Mayank Mehta, Lucia Melloni, Earl K. Miller, Bita Moghaddam, Hannah Monyer, Edvard I. Moser, May-Britt Moser, Danko Nikolic, William A. Phillips, Gordon Pipa, Constantin Rothkopf, Terrence J. Sejnowski, Steven M. Silverstein, Wolf Singer, Catherine Tallon-Baudry, Roger D. Traub, Jochen Triesch, Peter Uhlhaas, Christoph von der Malsburg, Thomas Weisswange, Miles Whittington, Matthew Wilson
An important characteristic of long-term potentiation (LTP) in the hippocampal CA1 region is that it is specific for those synapses which are active during the induction event. This input specificity ...is commonly attributed to the location and properties of the
N-methyl-
d-aspartate (NMDA) receptor channel. Experiments using strong high-frequency orthodromic activation have suggested that input-specific LTP can occur also in the absence of NMDA receptor activation. The present experiments have re-examined this question. They were performed in the CA1 region of hippocampal slices, and the synaptic strength was evaluated from the initial slope of the dendritically recorded field potential. In agreement with previous reports, 0.5 s. 200 Hz, orthodromic trains were found to lead to a substantial input-specific LTP (averaging 62%) in the presence of the competitive NMDA receptor antagonist
d-(−)-2-amino-5-phosphonopentanoic acid (
d-AP5) (20 μM). Under conditions of higher NMDA receptor blockade considerably less LTP was evoked. In 50 μM
d-AP5 and 20 μM chloro-kynurenate LTP averaged 13.4%, and after addition of 20 μM (+)-dizicilpine malcate (MK-801) LTP averaged 5.9%. On the other hand, in 20 μM
d-AP5 and 20 μM of the calcium channel antagonist nifedipine LTP averaged 49.9%. The present results suggest that NMDA receptor activity remaining in high concentrations of AP5 is sufficient to underly LTP induction under strong induction conditions.
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