Are there multiple visual short-term memory stores?

Sligte IG, Scholte HS, Lamme VA.
PLoS ONE. 2008 Feb 27;3(2):e1699.

BACKGROUND: Classic work on visual short-term memory (VSTM) suggests that people store a limited amount of items for subsequent report. However, when human observers are cued to shift attention to one item in VSTM during retention, it seems as if there is a much larger representation, which keeps additional items in a more fragile VSTM store. Thus far, it is not clear whether the capacity of this fragile VSTM store indeed exceeds the traditional capacity limits of VSTM. The current experiments address this issue and explore the capacity, stability, and duration of fragile VSTM representations. METHODOLOGY/PRINCIPAL FINDINGS: We presented cues in a change-detection task either just after off-set of the memory array (iconic-cue), 1,000 ms after off-set of the memory array (retro-cue) or after on-set of the probe array (post-cue). We observed three stages in visual information processing 1) iconic memory with unlimited capacity, 2) a four seconds lasting fragile VSTM store with a capacity that is at least a factor of two higher than 3) the robust and capacity-limited form of VSTM. Iconic memory seemed to depend on the strength of the positive after-image resulting from the memory display and was virtually absent under conditions of isoluminance or when intervening light masks were presented. This suggests that iconic memory is driven by prolonged retinal activation beyond stimulus duration. Fragile VSTM representations were not affected by light masks, but were completely overwritten by irrelevant pattern masks that spatially overlapped the memory array. CONCLUSIONS/SIGNIFICANCE: We find that immediately after a stimulus has disappeared from view, subjects can still access information from iconic memory because they can see an after-image of the display. After that period, human observers can still access a substantial, but somewhat more limited amount of information from a high-capacity, but fragile VSTM that is overwritten when new items are presented to the eyes. What is left after that is the traditional VSTM store, with a limit of about four objects. We conclude that human observers store more sustained representations than is evident from standard change detection tasks and that these representations can be accessed at will.

PMID: 18301775
Free Fulltext: http://www.plosone.org/article/info:doi/10.1371/journal.pone.0001699

Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field.

Monosov IE, Trageser JC, Thompson KG.
Neuron. 2008 Feb 28;57(4):614-25.

The frontal eye field (FEF) participates in selecting the location of behaviorally relevant stimuli for guiding attention and eye movements. We simultaneously recorded local field potentials (LFPs) and spiking activity in the FEF of monkeys performing memory-guided saccade and covert visual search tasks. We compared visual latencies and the time course of spatially selective responses in LFPs and spiking activity. Consistent with the view that LFPs represent synaptic input, visual responses appeared first in the LFPs followed by visual responses in the spiking activity. However, spatially selective activity identifying the location of the target in the visual search array appeared in the spikes about 30 ms before it appeared in the LFPs. Because LFPs reflect dendritic input and spikes measure neuronal output in a local brain region, this temporal relationship suggests that spatial selection necessary for attention and eye movements is computed locally in FEF from spatially nonselective inputs.

PMID: 18304489
Fulltext: http://download.neuron.org/pdfs/0896-6273/PIIS089662730800041X.pdf

Effects of Familiarity on Neural Activity in Monkey Inferior Temporal Lobe.

Anderson B, Mruczek RE, Kawasaki K, Sheinberg D.
Cereb Cortex. 2008 Feb 21

Long-term familiarity facilitates recognition of visual stimuli. To better understand the neural basis for this effect, we measured the local field potential (LFP) and multiunit spiking activity (MUA) from the inferior temporal (IT) lobe of behaving monkeys in response to novel and familiar images. In general, familiar images evoked larger amplitude LFPs whereas MUA responses were greater for novel images. Familiarity effects were attenuated by image rotations in the picture plane of 45 degrees . Decreasing image contrast led to more pronounced decreases in LFP response magnitude for novel, compared with familiar images, and resulted in more selective MUA response profiles for familiar images. The shape of individual LFP traces could be used for stimulus classification, and classification performance was better for the familiar image category. Recording the visual and auditory evoked LFP at multiple depths showed significant alterations in LFP morphology with distance changes of 2 mm. In summary, IT cortex shows local processing differences for familiar and novel images at a time scale and in a manner consistent with the observed behavioral advantage for classifying familiar images and rapidly detecting novel stimuli.

PMID: 18296433

Fulltext: http://cercor.oxfordjournals.org/cgi/content/full/bhn015v1

The spatiotemporal profile of cortical processing leading up to visual perception.

Fahrenfort JJ, Scholte HS, Lamme VA.
J Vis. 2008 Jan 21;8(1):12.1-12

Much controversy exists around the locus of conscious visual perception in human cortex. Some authors have proposed that its neural correlates correspond with recurrent processing within visual cortex, whereas others have argued they are located in a frontoparietal network. The present experiment aims to bring together these competing viewpoints. We recorded EEG from human subjects that were engaged in detecting masked visual targets. From this, we obtained a spatiotemporal profile of neural activity selectively related to the processing of the targets, which we correlated with the subjects' ability to detect those targets. This made it possible to distinguish between those stages of visual processing that correlate with human perception and those that do not. The results show that target induced extra-striate feedforward activity peaking at 121 ms does not correlate with perception, whereas more posterior recurrent activity peaking at 160 ms does. Several subsequent stages show an alternating pattern of frontoparietal and occipital activity, all of which correlate highly with perception. This shows that perception emerges early on, but only after an initial feedforward volley, and suggests that multiple reentrant loops are involved in propagating this signal to frontoparietal areas.

PMID: 18318615
Free Fulltext: http://journalofvision.org/8/1/12/Fahrenfort-2007-jov-8-1-12.pdf

Object features used by humans and monkeys to identify rotated shapes.

Nielsen KJ, Logothetis NK, Rainer G.
J Vis. 2008 Feb 22;8(2):9.1-15

Humans and rhesus monkeys can identify shapes that have been rotated in the picture plane. Recognition of rotated shapes can be as efficient as recognition of upright shapes. Here we investigate whether subjects showing view-invariant performance use the same object features to identify upright and rotated versions of a shape. We find marked differences between humans and monkeys. While humans tend to use the same features independent of shape orientation, monkeys use unique features for each orientation. Humans are able to generalize to a greater degree across orientation changes than rhesus monkey observers, who tend to relearn separate problems at each orientation rather than flexibly apply previously learned knowledge to novel problems.

PMID: 18318635
Free Fulltext: http://journalofvision.org/8/2/9/Nielsen-2008-jov-8-2-9.pdf

Stimulus selection via differential response latencies in visual cortical area V4.

Gawne TJ.
Neurosci Lett. 2008 Feb 26

Any given region of the cerebral cortex gets multiple inputs, and how these inputs are combined or selected is a key component of cortical function. Experiments in brain slices or other reduced preparations have shown that excitatory inputs to cortex produce a delayed feed-forward inhibition, which suggests that the relative timing of inputs at the scale of tens of milliseconds is crucial to cortical operation. Other mechanisms, such as synaptic depression and feedback inhibition, have also been shown to produce strong effects on this timescale. Thus, the relative timing of inputs should be fundamental in determining how a given region of cortex selects or combines its inputs. A rhesus monkey (Macaca mulatta) was trained to fixate on a spot of light for juice reward. Isolated single units in visual cortical area V4 were recorded using standard microelectrode techniques. Two visual stimuli were positioned such that each alone elicited a strong response. The stimuli were presented both separately and in combination, and their contrast and relative onset timing were varied. In general, the response of each neuron to two stimuli was locked to the response to that single stimulus that produced the shortest latency. A partial exception was that the responses to low-contrast stimuli were often less effective at suppressing later-arriving responses to high-contrast stimuli. The presentation of two stimuli in the receptive field of a visual cortical neuron is proposed as a model system for how changes in the relative timing of inputs affect cortical function in the intact system.

PMID: 18355960

Physiological differences between neurons in layer 2 and layer 3 of primary visual cortex (V1) of alert macaque monkeys.

Gur M, Snodderly DM.
J Physiol. 2008 Mar 6

The physiological literature does not distinguish between the superficial layers 2 and 3 of primary visual cortex even though these two layers differ in their cytoarchitecture and anatomical connections. To distinguish layer 2 from layer 3, we have analyzed the response characteristics of neurons recorded during microelectrode penetrations perpendicular to the cortical surface. Extracellular responses of single neurons to sweeping bars were recorded while macaque monkeys performed a fixation task. Data were analyzed from penetrations where cells could be localized to specific depths in the cortex. Although the most superficial cells (depth: 145-371 microm; presumably layer 2) responded preferentially to particular stimulus orientations, they were less selective than cells encountered immediately beneath them (depth: 386-696 microm; presumably layer 3). Layer 2 cells had smaller spikes, higher levels of ongoing activity, larger receptive field activating regions, and less finely tuned selectivity for stimulus orientation and length than layer 3 cells. Direction selectivity was found only in layer 3. These data suggest that layer 3 is involved in generating and transmitting precise, localized information about image features, while the lesser selectivity of layer 2 cells may reflect more global processing or top-down modulation of V1 by feedback from higher cortical areas.

PMID: 18325976

Fulltext: http://jp.physoc.org/cgi/rapidpdf/jphysiol.2008.151795v1

The Influence of Moderate Hypercapnia on Neural Activity in the Anesthetized Nonhuman Primate.

Zappe AC, Uludag K, Oeltermann A, Ugurbil K, Logothetis NK.
Cereb Cortex. 2008 Mar 10

Hypercapnia is often used as vasodilatory challenge in clinical applications and basic research. In functional magnetic resonance imaging (fMRI), elevated CO(2) is applied to derive stimulus-induced changes in the cerebral rate of oxygen consumption (CMRO(2)) by measuring cerebral blood flow and blood-oxygenation-level-dependent (BOLD) signal. Such methods, however, assume that hypercapnia has no direct effect on CMRO(2). In this study, we used combined intracortical recordings and fMRI in the visual cortex of anesthetized macaque monkeys to show that spontaneous neuronal activity is in fact significantly reduced by moderate hypercapnia. As expected, measurement of cerebral blood volume using an exogenous contrast agent and of BOLD signal showed that both are increased during hypercapnia. In contrast to this, spontaneous fluctuations of local field potentials in the beta and gamma frequency range as well as multiunit activity are reduced by approximately 15% during inhalation of 6% CO(2) (pCO(2) = 56 mmHg)(.) A strong tendency toward a reduction of neuronal activity was also found at CO(2) inhalation of 3% (pCO(2) = 45 mmHg). This suggests that CMRO(2) might be reduced during hypercapnia and caution must be exercised when hypercapnia is applied to calibrate the BOLD signal.

PMID: 18326521

Free Fulltext: http://cercor.oxfordjournals.org/cgi/reprint/bhn023v2.pdf

Phase-of-Firing Coding of Natural Visual Stimuli in Primary Visual Cortex

Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S.
Curr Biol. 2008 Mar 11;18(5):375-80.

We investigated the hypothesis that neurons encode rich naturalistic stimuli in terms of their spike times relative to the phase of ongoing network fluctuations rather than only in terms of their spike count. We recorded local field potentials (LFPs) and multiunit spikes from the primary visual cortex of anaesthetized macaques while binocularly presenting a color movie. We found that both the spike counts and the low-frequency LFP phase were reliably modulated by the movie and thus conveyed information about it. Moreover, movie periods eliciting higher firing rates also elicited a higher reliability of LFP phase across trials. To establish whether the LFP phase at which spikes were emitted conveyed visual information that could not be extracted by spike rates alone, we compared the Shannon information about the movie carried by spike counts to that carried by the phase of firing. We found that at low LFP frequencies, the phase of firing conveyed 54% additional information beyond that conveyed by spike counts. The extra information available in the phase of firing was crucial for the disambiguation between stimuli eliciting high spike rates of similar magnitude. Thus, phase coding may allow primary cortical neurons to represent several effective stimuli in an easily decodable format.

PMID: 18328702

ّFulltext: ScienceDirect

The distribution of category and location information across object-selective regions in human visual cortex.

Schwarzlose RF, Swisher JD, Dang S, Kanwisher N.
Proc Natl Acad Sci U S A. 2008 Mar 7

Since Ungerleider and Mishkin [Underleider LG, Mishkin M (1982) Two cortical visual systems. Analysis of Visual Behavior, eds Ingle MA, Goodale MI, Masfield RJW (MIT Press, Cambridge, MA), pp 549-586] proposed separate visual pathways for processing object shape and location, steady progress has been made in characterizing the organization of the two kinds of information in extrastriate visual cortex in humans. However, to date, there has been no broad-based survey of category and location information across all major functionally defined object-selective regions. In this study, we used an fMRI region-of-interest (ROI) approach to identify eight regions characterized by their strong selectivity for particular object categories (faces, scenes, bodies, and objects). Participants viewed four types of stimuli (faces, scenes, bodies, and cars) appearing in each of three different spatial locations (above, below, or at fixation). Analyses based on the mean response and voxelwise patterns of response in each ROI reveal location information in almost all of the known object-selective regions. Furthermore, category and location information can be read out independently of one another such that most regions contain both position-invariant category information and category-invariant position information. Finally, we find substantially more location information in ROIs on the lateral than those on the ventral surface of the brain, even though these regions have equal amounts of category information. Although the presence of both location and category information in most object-selective regions argues against a strict physical separation of processing streams for object shape and location, the ability to extract position-invariant category information and category-invariant position information from the same neural population indicates that form and location information nonetheless remain functionally independent.

PMID: 18326624

Fulltext: http://www.pnas.org/cgi/reprint/0800431105v1.pdf

Neural Dissociation between Visual Awareness and Spatial Attention

Valentin Wyart, and Catherine Tallon-Baudry
The Journal of Neuroscience, March 5, 2008, 28(10):2667-2679;

To what extent does what we consciously see depend on where we attend to? Psychologists have long stressed the tight relationship between visual awareness and spatial attention at the behavioral level. However, the amount of overlap between their neural correlates remains a matter of debate. We recorded magnetoencephalographic signals while human subjects attended toward or away from faint stimuli that were reported as consciously seen only half of the time. Visually identical stimuli could thus be attended or not and consciously seen or not. Although attended stimuli were consciously seen slightly more often than unattended ones, the factorial analysis of stimulus-induced oscillatory brain activity revealed distinct and independent neural correlates of visual awareness and spatial attention at different frequencies in the gamma range (30–150 Hz). Whether attended or not, consciously seen stimuli induced increased mid-frequency gamma-band activity over the contralateral visual cortex, whereas spatial attention modulated high-frequency gamma-band activity in response to both consciously seen and unseen stimuli. A parametric analysis of the data at the single-trial level confirmed that the awareness-related mid-frequency activity drove the seen–unseen decision but also revealed a small influence of the attention-related high-frequency activity on the decision. These results suggest that subjective visual experience is shaped by the cumulative contribution of two processes operating independently at the neural level, one reflecting visual awareness per se and the other reflecting spatial attention.

Fulltext: http://www.jneurosci.org/cgi/reprint/28/10/2667

A Hierarchy of Temporal Receptive Windows in Human Cortex

Uri Hasson, Eunice Yang, Ignacio Vallines, David J. Heeger, and Nava Rubin
The Journal of Neuroscience, March 5, 2008, 28(10):2539-2550

Real-world events unfold at different time scales and, therefore, cognitive and neuronal processes must likewise occur at different time scales. We present a novel procedure that identifies brain regions responsive to sensory information accumulated over different time scales. We measured functional magnetic resonance imaging activity while observers viewed silent films presented forward, backward, or piecewise-scrambled in time. Early visual areas (e.g., primary visual cortex and the motion-sensitive area MT+) exhibited high response reliability regardless of disruptions in temporal structure. In contrast, the reliability of responses in several higher brain areas, including the superior temporal sulcus (STS), precuneus, posterior lateral sulcus (LS), temporal parietal junction (TPJ), and frontal eye field (FEF), was affected by information accumulated over longer time scales. These regions showed highly reproducible responses for repeated forward, but not for backward or piecewise-scrambled presentations. Moreover, these regions exhibited marked differences in temporal characteristics, with LS, TPJ, and FEF responses depending on information accumulated over longer durations (~36 s) than STS and precuneus (~12 s). We conclude that, similar to the known cortical hierarchy of spatial receptive fields, there is a hierarchy of progressively longer temporal receptive windows in the human brain.

Fulltext: http://www.jneurosci.org/cgi/reprint/28/10/2539

Neuronal Selectivity and Local Map Structure in Visual Cortex

Ian Nauhaus, Andrea Benucci, Matteo Carandini and Dario L. Ringach
Neuron, Volume 57, Issue 5, 13 March 2008, Pages 673-679

The organization of primary visual cortex (V1) into functional maps makes individual cells operate in a variety of contexts. For instance, some neurons lie in regions of fairly homogeneous orientation preference (iso-orientation domains), while others lie in regions with a variety of preferences (e.g., pinwheel centers). We asked whether this diversity in local map structure correlates with the degree of selectivity of spike responses. We used a combination of imaging and electrophysiology to reveal that neurons in regions of homogeneous orientation preference have much sharper tuning. Moreover, in both monkeys and cats, a common principle links the structure of the orientation map, on the spatial scale of dendritic integration, to the degree of selectivity of individual cells. We conclude that neural computation is not invariant across the cortical surface. This finding must factor into future theories of receptive field wiring and map development.

Fulltext: ScienceDirect