Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information.

Belitski A, Gretton A, Magri C, Murayama Y, Montemurro MA, Logothetis NK, Panzeri S.
J Neurosci. 2008 May 28;28(22):5696-709.

Local field potentials (LFPs) reflect subthreshold integrative processes that complement spike train measures. However, little is yet known about the differences between how LFPs and spikes encode rich naturalistic sensory stimuli. We addressed this question by recording LFPs and spikes from the primary visual cortex of anesthetized macaques while presenting a color movie. We then determined how the power of LFPs and spikes at different frequencies represents the visual features in the movie. We found that the most informative LFP frequency ranges were 1-8 and 60-100 Hz. LFPs in the range of 12-40 Hz carried little information about the stimulus, and may primarily reflect neuromodulatory inputs. Spike power was informative only at frequencies <12 Hz. We further quantified "signal correlations" (correlations in the trial-averaged power response to different stimuli) and "noise correlations" (trial-by-trial correlations in the fluctuations around the average) of LFPs and spikes recorded from the same electrode. We found positive signal correlation between high-gamma LFPs (60-100 Hz) and spikes, as well as strong positive signal correlation within high-gamma LFPs, suggesting that high-gamma LFPs and spikes are generated within the same network. LFPs <24 Hz shared strong positive noise correlations, indicating that they are influenced by a common source, such as a diffuse neuromodulatory input. LFPs <40 Hz showed very little signal and noise correlations with LFPs >40 Hz and with spikes, suggesting that low-frequency LFPs reflect neural processes that in natural conditions are fully decoupled from those giving rise to spikes and to high-gamma LFPs.

PMID: 18509031

Fulltext: http://www.jneurosci.org/cgi/reprint/28/22/5696

Nature NeuroTechniques

http://www.nature.com/focus/neurotechniques/index.html

Imagine Jane and Identify John: Face Identity Aftereffects Induced by Imagined Faces

Jae-Jin Ryu, Karen Borrmann, Avi Chaudhuri
PlosOne

It is not known whether prolonged exposure to perceived and imagined complex visual images produces similar shifts in subsequent perception through selective adaptation. This question is important because a positive finding would suggest that perception and imagery of visual stimuli are mediated by shared neural networks. In this study, we used a selective adaptation procedure designed to induce high-level face-identity aftereffects—a phenomenon in which extended exposure to a particular face facilitates recognition of subsequent faces with opposite features while impairing recognition of all other faces. We report here that adaptation to either real or imagined faces produces a similar shift in perception and that identity boundaries represented in real and imagined faces are equivalent. Together, our results show that identity information contained in imagined and real faces produce similar behavioral outcomes. Our findings of high-level visual aftereffects induced by imagined stimuli can be taken as evidence for the involvement of shared neural networks that mediate perception and imagery of complex visual stimuli.

Free Fulltext: PlosOne

A Map for Horizontal Disparity in Monkey V2

Gang Chen, Haidong D. Lu, Anna W. Roe
Volume 58, Issue 3, 8 May 2008, Pages 442-450

The perception of visual depth is determined by integration of spatial disparities of inputs from the two eyes. Single cells in visual cortex of monkeys are known to respond to specific binocular disparities; however, little is known about their functional organization. We now show, using intrinsic signal optical imaging and single-unit physiology, that, in the thick stripe compartments of the second visual area (V2), there is a clustered organization of Near cells and Far cells, and moreover, there are topographic maps for Near to Far disparities within V2. Our findings suggest that maps for visual disparity are calculated in V2, and demonstrate parallels in functional organization between the thin, pale, and thick stripes of V2.

Fulltext: ScienceDirect

Saccadic latency during electrical stimulation of the human subthalamic nucleus

Yasin Temel, Veerle Visser-Vandewalle, R.H.S. Carpenter
Current Biology, Vol 18, R412-R414, 20 May 2008

High-frequency electrical stimulation of the subthalamic nucleus (‘deep brain stimulation’) has rapidly become a popular method for treating patients with Parkinson's disease [1], and is now widely recognised as one of the most effective long-term treatments. So far, the neural mechanisms underlying its effectiveness have been elusive. However, measuring saccadic latency — the time taken to look at a sudden visual stimulus — seems a promising approach. Latency varies randomly from trial to trial, and analysis of the resultant statistical distributions provides information about the parameters of the underlying decision-making mechanisms of the brain. Measurement of these parameters can then provide a sensitive and non-invasive way of quantifying the effects of clinical interventions, and providing information about the underlying neural mechanisms. In a group of Parkinson patients with electrodes previously implanted in the subthalamic nuclear complex, we found that bilateral electrical stimulation dramatically reduces the time taken to initiate a saccade. The effect on the distribution of latency corresponds to an increase in the rate of accumulation of the underlying decision signal, suggesting that stimulating this region specifically enhances the gain of descending pathways through the basal ganglia that contribute to saccadic initiation.

Fulltext: http://download.current-biology.com/pdfs/0960-9822/PIIS0960982208003059.pdf

Prefrontal-inferotemporal interaction is not always necessary for reversal learning.

Wilson CR, Gaffan D.
J Neurosci. 2008 May 21;28(21):5529-38.

Prefrontal cortex (PFC) is thought to have a wide-ranging role in cognition, often described as executive function or behavioral inhibition. A specific example of such a role is the inhibition of representations in more posterior regions of cortex in a "top-down" manner, a function thought to be tested by reversal learning tasks. The direct action of PFC on posterior regions can be directly tested by disconnecting PFC from the region in question. We tested whether PFC directly inhibits visual object representations in inferotemporal cortex (IT) during reversal learning by studying the effect, in macaque monkeys, of disconnecting PFC from IT by crossed unilateral ablations. We tested two visual object reversal learning tasks, namely serial and concurrent reversal learning. We found that the disconnection severely impairs serial reversal learning but leaves concurrent reversal learning completely intact. Thus, PFC cannot be said to always have direct inhibitory control over visual object representations in reversal learning. Furthermore, our results cannot be explained by generalized theories of PFC function such as executive function and behavioral inhibition, because those theories do not make predictions that differentiate different forms of reversal learning. The results do, however, support our proposal, based on other experimental evidence from macaque monkeys, that PFC has a highly specific role in the representation of temporally complex events.

PMID: 18495887

Fulltext: http://www.jneurosci.org/cgi/reprint/28/21/5529

Decision-making with multiple alternatives.

Churchland AK, Kiani R, Shadlen MN.
Nat Neurosci. 2008 May 18.

Simple perceptual tasks have laid the groundwork for understanding the neurobiology of decision-making. Here, we examined this foundation to explain how decision-making circuitry adjusts in the face of a more difficult task. We measured behavioral and physiological responses of monkeys on a two- and four-choice direction-discrimination decision task. For both tasks, firing rates in the lateral intraparietal area appeared to reflect the accumulation of evidence for or against each choice. Evidence accumulation began at a lower firing rate for the four-choice task, but reached a common level by the end of the decision process. The larger excursion suggests that the subjects required more evidence before making a choice. Furthermore, on both tasks, we observed a time-dependent rise in firing rates that may impose a deadline for deciding. These physiological observations constitute an effective strategy for handling increased task difficulty. The differences appear to explain subjects' accuracy and reaction times.

PMID: 18488024

The neural systems that mediate human perceptual decision making

Hauke R. Heekeren, Sean Marrett & Leslie G. Ungerleider
Nature Reviews Neuroscience 9, 467-479 (June 2008) | doi:10.1038/nrn2374

Heekeren and colleagues review neurophysiological and neuroimaging studies of monkeys and humans making perceptual decisions, highlighting both the similarities and the differences in their decision-making processes and providing a new model for the neural architecture that underlies perceptual decision making in humans.

Fulltext: http://www.nature.com/nrn/journal/v9/n6/pdf/nrn2374.pdf

Fragment-Based Learning of Visual Object Categories

Jay Hegdé, Evgeniy Bart, Daniel Kersten
Current Biology, Vol 18, 597-601, 22 April 2008

When we perceive a visual object, we implicitly or explicitly associate it with a category we know [1, 2, 3]. It is known that the visual system can use local, informative image fragments of a given object, rather than the whole object, to classify it into a familiar category [4, 5, 6, 7, 8]. How we acquire informative fragments has remained unclear. Here, we show that human observers acquire informative fragments during the initial learning of categories. We created new, but naturalistic, classes of visual objects by using a novel “virtual phylogenesis” (VP) algorithm that simulates key aspects of how biological categories evolve. Subjects were trained to distinguish two of these classes by using whole exemplar objects, not fragments. We hypothesized that if the visual system learns informative object fragments during category learning, then subjects must be able to perform the newly learned categorization by using only the fragments as opposed to whole objects. We found that subjects were able to successfully perform the classification task by using each of the informative fragments by itself, but not by using any of the comparable, but uninformative, fragments. Our results not only reveal that novel categories can be learned by discovering informative fragments but also introduce and illustrate the use of VP as a versatile tool for category-learning research.

Fulltext: http://download.current-biology.com/pdfs/0960-9822/PIIS096098220800448X.pdf

Electrical microstimulation thresholds for behavioral detection and saccades in monkey frontal eye fields.

Murphey DK, Maunsell JH
Proc Natl Acad Sci U S A. 2008 May 13.

The frontal eye field (FEF) is involved in the transformation of visual signals into saccadic eye movements. Although it is often considered an oculomotor structure, several lines of evidence suggest that the FEF also contributes to visual perception and attention. To better understand the range of behaviors to which the FEF can contribute, we tested whether monkeys could detect activation of their FEF by electrical microstimulation with currents below those that cause eye movements. We found that stimulation of FEF neurons could almost always be detected at levels below those needed to generate saccades and that the electrical current needed for detection was highly correlated with that needed to generate a saccade. This relationship between detection and saccade thresholds can be explained if FEF neurons represent preparation to make particular saccades and subjects can be aware of such preparations without acting on them when the representation is not strong.

PMID: 18477698

Free Fulltext: http://www.pnas.org/cgi/reprint/0710820105v1

Electric stimulation fMRI of the perforant pathway to the rat hippocampus

Canals S, Beyerlein M, Murayama Y, Logothetis NK.
Magn Reson Imaging. 2008 May 12.

The hippocampal formation is a brain system that is implicated in learning and memory. The major input to the hippocampus arrives from the entorhinal cortex (EC) to the dentate gyrus (DG) through the perforant path. In the present work, we have investigated the functional properties of this connection by concomitantly applying electrophysiological techniques, deep-brain electric microstimulation and functional magnetic resonance imaging in anesthetized rats. We systematically delivered different current intensities at diverse stimulation frequencies to the perforant path while recording electrophysiological and blood-oxygenation-level-dependent (BOLD) signals. We observed a linear relationship between the current intensity used to stimulate the hippocampal formation and the amplitude and extension of the induced BOLD response. In addition, we found a frequency-dependent spatial pattern of activation. With stimulation protocols and train frequencies used for kindling, the activity strongly spreads ipsilaterally through the hippocampus, DG, subiculum and EC.

PMID: 18479870

Fulltext: ScienceDirect

PhD Comics

Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades

Shlomit Yuval-Greenberg, Orr Tomer, Alon S. Keren, Israel Nelken, Leon Y. Deouell
Neuron, Vol 58, 429-441, 08 May 2008

The induced gamma-band EEG response (iGBR) recorded on the scalp is widely assumed to reflect synchronous neural oscillation associated with object representation, attention, memory, and consciousness. The most commonly reported EEG iGBR is a broadband transient increase in power at the gamma range ∼200–300 ms following stimulus onset. A conspicuous feature of this iGBR is the trial-to-trial poststimulus latency variability, which has been insufficiently addressed. Here, we show, using single-trial analysis of concomitant EEG and eye tracking, that this iGBR is tightly time locked to the onset of involuntary miniature eye movements and reflects a saccadic “spike potential.” The time course of the iGBR is related to an increase in the rate of saccades following a period of poststimulus saccadic inhibition. Thus, whereas neuronal gamma-band oscillations were shown conclusively with other methods, the broadband transient iGBR recorded by scalp EEG reflects properties of miniature saccade dynamics rather than neuronal oscillations.

Fulltext: http://download.neuron.org/pdfs/0896-6273/PIIS0896627308003012.pdf

The neural systems that mediate human perceptual decision making

Heekeren HR, Marrett S, Ungerleider LG.
Nat Rev Neurosci. 2008 May 9

Perceptual decision making is the act of choosing one option or course of action from a set of alternatives on the basis of available sensory evidence. Thus, when we make such decisions, sensory information must be interpreted and translated into behaviour. Neurophysiological work in monkeys performing sensory discriminations, combined with computational modelling, has paved the way for neuroimaging studies that are aimed at understanding decision-related processes in the human brain. Here we review findings from human neuroimaging studies in conjunction with data analysis methods that can directly link decisions and signals in the human brain on a trial-by-trial basis. This leads to a new view about the neural basis of human perceptual decision-making processes.

PMID: 18464792

Short-term memory trace in rapidly adapting synapses of inferior temporal cortex

Sugase-Miyamoto Y, Liu Z, Wiener MC, Optican LM, Richmond BJ.
PLoS Comput Biol. 2008 May 9;4(5):e1000073.

Visual short-term memory tasks depend upon both the inferior temporal cortex (ITC) and the prefrontal cortex (PFC). Activity in some neurons persists after the first (sample) stimulus is shown. This delay-period activity has been proposed as an important mechanism for working memory. In ITC neurons, intervening (nonmatching) stimuli wipe out the delay-period activity; hence, the role of ITC in memory must depend upon a different mechanism. Here, we look for a possible mechanism by contrasting memory effects in two architectonically different parts of ITC: area TE and the perirhinal cortex. We found that a large proportion (80%) of stimulus-selective neurons in area TE of macaque ITCs exhibit a memory effect during the stimulus interval. During a sequential delayed matching-to-sample task (DMS), the noise in the neuronal response to the test image was correlated with the noise in the neuronal response to the sample image. Neurons in perirhinal cortex did not show this correlation. These results led us to hypothesize that area TE contributes to short-term memory by acting as a matched filter. When the sample image appears, each TE neuron captures a static copy of its inputs by rapidly adjusting its synaptic weights to match the strength of their individual inputs. Input signals from subsequent images are multiplied by those synaptic weights, thereby computing a measure of the correlation between the past and present inputs. The total activity in area TE is sufficient to quantify the similarity between the two images. This matched filter theory provides an explanation of what is remembered, where the trace is stored, and how comparison is done across time, all without requiring delay period activity. Simulations of a matched filter model match the experimental results, suggesting that area TE neurons store a synaptic memory trace during short-term visual memory.

PMID: 18464917

Free Fulltext: http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000073

Value Representations in the Primate Striatum during Matching Behavior.

Lau B, Glimcher PW.
Neuron. 2008 May 8;58(3):451-63.

Choosing the most valuable course of action requires knowing the outcomes associated with the available alternatives. The striatum may be important for representing the values of actions. We examined this in monkeys performing an oculomotor choice task. The activity of phasically active neurons (PANs) in the striatum covaried with two classes of information: action-values and chosen-values. Action-value PANs were correlated with value estimates for one of the available actions, and these signals were frequently observed before movement execution. Chosen-value PANs were correlated with the value of the action that had been chosen, and these signals were primarily observed later in the task, immediately before or persistently after movement execution. These populations may serve distinct functions mediated by the striatum: some PANs may participate in choice by encoding the values of the available actions, while other PANs may participate in evaluative updating by encoding the reward value of chosen actions.

PMID: 18466754

Fulltext: http://download.neuron.org/pdfs/0896-6273/PIIS089662730800175X.pdf

Learning to recognize visual objects with microstimulation in inferior temporal cortex

Kawasaki K, Sheinberg DL.
J Neurophysiol. 2008 May 7

The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can neither be explained by direct stimulation-motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation, as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations.

PMID: 18463185

Fulltext: http://jn.physiology.org/cgi/reprint/90247.2008v1

Spatial summation can explain the attentional modulation of neuronal responses to multiple stimuli in area V4.

Ghose GM, Maunsell JH.
J Neurosci. 2008 May 7;28(19):5115-26

Although many studies have shown that the activity of individual neurons in a variety of visual areas is modulated by attention, a fundamental question remains unresolved: can attention alter the visual representations of individual neurons? One set of studies, primarily relying on the attentional modulations observed when a single stimulus is presented within the receptive field of a neuron, suggests that neuronal selectivities, such as orientation or direction tuning, are not fundamentally altered by attention (Salinas and Abbott, 1997; McAdams and Maunsell, 1999; Treue and Martinez Trujillo, 1999). Another set of studies, relying on modulations observed when multiple stimuli are presented within a receptive field, suggests that attention can alter the weighting of sensory inputs (Moran and Desimone, 1985; Luck et al., 1997; Reynolds et al., 1999; Chelazzi et al., 2001). In these studies, when preferred and nonpreferred stimuli are simultaneously presented, responses are much stronger when attention is directed to the preferred stimulus than when it is directed to the nonpreferred stimulus. In this study, we recorded neuronal responses from individual neurons in visual cortical area V4 to both single and paired stimuli with a variety of attentional allocations and stimulus combinations. For each neuron studied, we constructed a quantitative model of input summation and then tested various models of attention. In many neurons, we are able to explain neuronal responses across the entire range of stimuli and attentional allocations tested. Specifically, we are able to reconcile seemingly inconsistent observations of single and paired stimuli attentional modulation with a new model in which attention can facilitate or suppress specific inputs to a neuron but does not fundamentally alter the integration of these inputs.

PMID: 18463265

Interactions between the superior temporal sulcus and auditory cortex mediate dynamic face/voice integration in rhesus monkeys

Ghazanfar AA, Chandrasekaran C, Logothetis NK.
J Neurosci. 2008 Apr 23;28(17):4457-69

The existence of multiple nodes in the cortical network that integrate faces and voices suggests that they may be interacting and influencing each other during communication. To test the hypothesis that multisensory responses in auditory cortex are influenced by visual inputs from the superior temporal sulcus (STS), an association area, we recorded local field potentials and single neurons from both structures concurrently in monkeys. The functional interactions between the auditory cortex and the STS, as measured by spectral analyses, increased in strength during presentations of dynamic faces and voices relative to either communication signal alone. These interactions were not solely modulations of response strength, because the phase relationships were significantly less variable in the multisensory condition as well. A similar analysis of functional interactions within the auditory cortex revealed no similar interactions as a function of stimulus condition, nor did a control condition in which the dynamic face was replaced with a dynamic disk mimicking mouth movements. Single neuron data revealed that these intercortical interactions were reflected in the spiking output of auditory cortex and that such spiking output was coordinated with oscillations in the STS. The vast majority of single neurons that were responsive to voices showed integrative responses when faces, but not control stimuli, were presented in conjunction. Our data suggest that the integration of faces and voices is mediated at least in part by neuronal cooperation between auditory cortex and the STS and that interactions between these structures are a fast and efficient way of dealing with the multisensory communication signals.

PMID: 1843452

Fulltext: http://www.jneurosci.org/cgi/reprint/28/17/4457

The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4.

Fries P, Womelsdorf T, Oostenveld R, Desimone R.
J Neurosci. 2008 Apr 30;28(18):4823-35

Selective attention lends relevant sensory input priority access to higher-level brain areas and ultimately to behavior. Recent studies have suggested that those neurons in visual areas that are activated by an attended stimulus engage in enhanced gamma-band (30-70 Hz) synchronization compared with neurons activated by a distracter. Such precise synchronization could enhance the postsynaptic impact of cells carrying behaviorally relevant information. Previous studies have used the local field potential (LFP) power spectrum or spike-LFP coherence (SFC) to indirectly estimate spike synchronization. Here, we directly demonstrate zero-phase gamma-band coherence among spike trains of V4 neurons. This synchronization was particularly evident during visual stimulation and enhanced by selective attention, thus confirming the pattern inferred from LFP power and SFC. We therefore investigated the time course of LFP gamma-band power and found rapid dynamics consistent with interactions of top-down spatial and feature attention with bottom-up saliency. In addition to the modulation of synchronization during visual stimulation, selective attention significantly changed the prestimulus pattern of synchronization. Attention inside the receptive field of the recorded neuronal population enhanced gamma-band synchronization and strongly reduced alpha-band (9-11 Hz) synchronization in the prestimulus period. These results lend further support for a functional role of rhythmic neuronal synchronization in attentional stimulus selection.

PMID: 18448659
Fulltext: http://www.jneurosci.org/cgi/reprint/28/18/4823

Neurophysiology of the BOLD fMRI Signal in Awake Monkeys

Goense JB, Logothetis NK.
Curr Biol. 2008 Apr 23

BACKGROUND: Simultaneous intracortical recordings of neural activity and blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (fMRI) in primary visual cortex of anesthetized monkeys demonstrated varying degrees of correlation between fMRI signals and the different types of neural activity, such as local field potentials (LFPs), multiple-unit activity (MUA), and single-unit activity (SUA). One important question raised by the aforementioned investigation is whether the reported correlations also apply to alert subjects. RESULTS: Monkeys were trained to perform a fixation task while stimuli within the receptive field of each recording site were used to elicit neural responses followed by a BOLD response. We show - also in alert behaving monkeys - that although both LFP and MUA make significant contributions to the BOLD response, LFPs are better and more reliable predictors of the BOLD signal. Moreover, when MUA responses adapt but LFP remains unaffected, the BOLD signal remains unaltered. CONCLUSIONS: The persistent coupling of the BOLD signal to the field potential when LFP and MUA have different time evolutions suggests that BOLD is primarily determined by the local processing of inputs in a given cortical area. In the alert animal the largest portion of the BOLD signal's variance is explained by an LFP range (20-60 Hz) that is most likely related to neuromodulation. Finally, the similarity of the results in alert and anesthetized subjects indicates that at least in V1 anesthesia is not a confounding factor. This enables the comparison of human fMRI results with a plethora of electrophysiological results obtained in alert or anesthetized animals.

PMID: 18439825

Fulltext: Science Direct