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2.  Local field potentials reflect multiple spatial scales in V4 
Local field potentials (LFP) reflect the properties of neuronal circuits or columns recorded in a volume around a microelectrode (Buzsáki et al., 2012). The extent of this integration volume has been a subject of some debate, with estimates ranging from a few hundred microns (Katzner et al., 2009; Xing et al., 2009) to several millimeters (Kreiman et al., 2006). We estimated receptive fields (RFs) of multi-unit activity (MUA) and LFPs at an intermediate level of visual processing, in area V4 of two macaques. The spatial structure of LFP receptive fields varied greatly as a function of time lag following stimulus onset, with the retinotopy of LFPs matching that of MUAs at a restricted set of time lags. A model-based analysis of the LFPs allowed us to recover two distinct stimulus-triggered components: an MUA-like retinotopic component that originated in a small volume around the microelectrodes (~350 μm), and a second component that was shared across the entire V4 region; this second component had tuning properties unrelated to those of the MUAs. Our results suggest that the LFP reflects neural activity across multiple spatial scales, which both complicates its interpretation and offers new opportunities for investigating the large-scale structure of network processing.
doi:10.3389/fncom.2013.00021
PMCID: PMC3607798  PMID: 23533106
receptive field; multiunit activity; local field potentials; V4; visual cortex
3.  Perisaccadic Remapping and Rescaling of Visual Responses in Macaque Superior Colliculus 
PLoS ONE  2012;7(12):e52195.
Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.
doi:10.1371/journal.pone.0052195
PMCID: PMC3524080  PMID: 23284931
4.  Parietal Cortex Signals Come Unstuck in Time 
PLoS Biology  2012;10(10):e1001414.
Humans and other animals are surprisingly adept at estimating the duration of temporal intervals, even without the use of watches and clocks. This ability is typically studied in the lab by asking observers to indicate their estimate of the time between two external sensory events. The results of such studies confirm that humans can accurately estimate durations on a variety of time scales. Although many brain areas are thought to contribute to the representation of elapsed time, recent neurophysiological studies have linked the parietal cortex in particular to the perception of sub-second time intervals. In this Primer, we describe previous work on parietal cortex and time perception, and we highlight the findings of a study published in this issue of PLOS Biology, in which Schneider and Ghose [1] characterize single-neuron responses during performance of a novel “Temporal Production” task. During temporal production, the observer must track the passage of time without anticipating any external sensory event, and it appears that the parietal cortex may use a unique strategy to support this type of measurement.
doi:10.1371/journal.pbio.1001414
PMCID: PMC3484121  PMID: 23118615
5.  The Rates of Protein Synthesis and Degradation Account for the Differential Response of Neurons to Spaced and Massed Training Protocols 
PLoS Computational Biology  2011;7(12):e1002324.
The sensory-motor neuron synapse of Aplysia is an excellent model system for investigating the biochemical changes underlying memory formation. In this system, training that is separated by rest periods (spaced training) leads to persistent changes in synaptic strength that depend on biochemical pathways that are different from those that occur when the training lacks rest periods (massed training). Recently, we have shown that in isolated sensory neurons, applications of serotonin, the neurotransmitter implicated in inducing these synaptic changes during memory formation, lead to desensitization of the PKC Apl II response, in a manner that depends on the method of application (spaced versus massed). Here, we develop a mathematical model of this response in order to gain insight into how neurons sense these different training protocols. The model was developed incrementally, and each component was experimentally validated, leading to two novel findings: First, the increased desensitization due to PKA-mediated heterologous desensitization is coupled to a faster recovery than the homologous desensitization that occurs in the absence of PKA activity. Second, the model suggests that increased spacing leads to greater desensitization due to the short half-life of a hypothetical protein, whose production prevents homologous desensitization. Thus, we predict that the effects of differential spacing are largely driven by the rates of production and degradation of proteins. This prediction suggests a powerful mechanism by which information about time is incorporated into neuronal processing.
Author Summary
Memories are among an individual's most cherished possessions. One factor that has been shown to exert a powerful influence on memory formation is the pattern of training. Learning trials distributed over time have been shown to consistently produce longer lasting memories than trials distributed over short intervals, in every organism in which this has been studied. This observation has been investigated particularly well in the marine mollusk Aplysia californica. The nervous system of Aplysia is simple and well characterized, yet capable of forming memories, making it an ideal system for the study of learning and memory. Currently, we have a detailed understanding of memory formation in Aplysia at the cellular level. However, there remain many unanswered questions at the molecular level, particularly concerning how the effects of different patterns of learning are mediated. We have developed a mathematical model of a molecular signaling pathway known to underlie memory formation in Aplysia. Our model suggests that the rates of synthesis and degradation of proteins involved in memory regulation are essential for neurons of Aplysia to respond differentially to spaced and massed training. We were able to experimentally validate these findings, thus providing significant evidence for this model, which might underlie memory formation in more complex animals.
doi:10.1371/journal.pcbi.1002324
PMCID: PMC3248386  PMID: 22219722
6.  Contributions of Indirect Pathways to Visual Response Properties in Macaque Area MT 
The primate visual cortex exhibits a remarkable degree of interconnectivity. Each visual area receives an average of ten to fifteen inputs, many of them from cortical areas with overlapping, but not identical, functional properties. In this study, we assessed the functional significance of this anatomical parallelism to the middle temporal area (MT) of the macaque visual cortex. MT receives major feedforward inputs from areas V1, V2 and V3, but little is known about the properties of each of these pathways. We previously demonstrated that reversible inactivation of V2 and V3 causes a disproportionate degradation of tuning for binocular disparity of MT neurons, relative to direction tuning (Ponce et al., 2008). Here we show that MT neurons continued to encode speed and size information during V2/3 inactivation; however, many became significantly less responsive to fast speeds and others showed a modest decrease in surround suppression. These changes resemble previously reported effects of reducing stimulus contrast (Pack et al., 2005; Krekelberg et al., 2006), but we show here that they differ in their temporal dynamics. We find no evidence that the indirect pathways selectively target different functional regions within MT. Overall, our findings suggest that the indirect pathways to MT primarily convey modality-specific information on binocular disparity, but that they also contribute to the processing of stimuli moving at fast speeds.
doi:10.1523/JNEUROSCI.5362-10.2011
PMCID: PMC3117290  PMID: 21389244
7.  Improved Discrimination of Visual Stimuli Following Repetitive Transcranial Magnetic Stimulation 
PLoS ONE  2010;5(4):e10354.
Background
Repetitive transcranial magnetic stimulation (rTMS) at certain frequencies increases thresholds for motor-evoked potentials and phosphenes following stimulation of cortex. Consequently rTMS is often assumed to introduce a “virtual lesion” in stimulated brain regions, with correspondingly diminished behavioral performance.
Methodology/Principal Findings
Here we investigated the effects of rTMS to visual cortex on subjects' ability to perform visual psychophysical tasks. Contrary to expectations of a visual deficit, we find that rTMS often improves the discrimination of visual features. For coarse orientation tasks, discrimination of a static stimulus improved consistently following theta-burst stimulation of the occipital lobe. Using a reaction-time task, we found that these improvements occurred throughout the visual field and lasted beyond one hour post-rTMS. Low-frequency (1 Hz) stimulation yielded similar improvements. In contrast, we did not find consistent effects of rTMS on performance in a fine orientation discrimination task.
Conclusions/Significance
Overall our results suggest that rTMS generally improves or has no effect on visual acuity, with the nature of the effect depending on the type of stimulation and the task. We interpret our results in the context of an ideal-observer model of visual perception.
doi:10.1371/journal.pone.0010354
PMCID: PMC2860988  PMID: 20442776
8.  Spatiotemporal Structure of Nonlinear Subunits in Macaque Visual Cortex 
The primate visual system is arranged hierarchically, starting from the retina and continuing through a series of extrastriate visual areas. Selectivity for motion is first found in individual neurons in the primate visual cortex (V1), in which many simple cells respond selectively to the direction and speed of moving stimuli. Beyond simple cells, most studies of direction selectivity have focused on either V1 complex cells or neurons in the middle temporal area (MT/V5). To understand how visual information is transferred along this pathway, we have studied all three types of neurons, using a reverse correlation procedure to obtain high spatial and temporal resolution maps of activity for different motion stimuli. Most complex and MT cells showed strong second-order interactions, indicating that they were tuned for particular displacements of an apparent motion stimulus. The spatiotemporal structure of these interactions showed a high degree of similarity between the populations of V1 complex cells and MT cells, in terms of the spatiotemporal limits and preferences for motion and their two-dimensional spatial structure. Much of the structure in the V1 and MT second-order kernels could be accounted for on the basis of the first-order responses of V1 simple cells, under the assumption of a Reichardt or motion-energy type of computation.
doi:10.1523/JNEUROSCI.3226-05.2006
PMCID: PMC1413500  PMID: 16421309
cortex; MT; striate cortex; vision; visual; computation
9.  Neural basis for a powerful static motion illusion 
doi:10.1523/JNEUROSCI.1084-05.2005
PMCID: PMC1431688  PMID: 15944393
Reverse-phi motion; visual illusion; V1; MT; direction-selectivity. Primate; striate Cortex

Results 1-9 (9)