Integrating what and when across the primate medial temporal lobe

Episodic memory or memory for the detailed events in our lives is critically dependent on structures of the medial temporal lobe (MTL). A fundamental component of episodic memory is memory for the temporal order of items within an episode. To understand the contribution of individual MTL structures to temporal-order memory, we recorded single-unit activity and local field potential from three MTL areas (hippocampus and entorhinal and perirhinal cortex) and visual area TE as monkeys performed a temporal-order memory task. Hippocampus provided incremental timing signals from one item presentation to the next, whereas perirhinal cortex signaled the conjunction of items and their relative temporal order. Thus, perirhinal cortex appeared to integrate timing information from hippocampus with item information from visual sensory area TE.     

A neural mechanism for working and recognition memory in inferior temporal cortex

Inferior temporal (IT) cortex is critical for visual memory, but it is not known how IT neurons retain memories while new information is streaming into the visual system. Single neurons were therefore recorded from IT cortex of two rhesus monkeys performing tasks that required them to hold items in memory while concurrently viewing other items. The neuronal response to an incoming visual stimulus was attenuated if it matched a stimulus actively held in working memory, even when several other stimuli intervened. The neuronal response to novel stimuli declined as the stimuli became familiar to the animal. IT neurons appear to function as adaptive mnemonic "filters" that preferentially pass information about new, unexpected, or not recently seen stimuli.     

Reversal of interlaminar signal between sensory and memory processing in monkey temporal cortex

The primate temporal cortex implements visual long-term memory. However, how its interlaminar circuitry executes cognitive computations is poorly understood. Using linear-array multicontact electrodes, we simultaneously recorded unit activities across cortical layers in the perirhinal cortex of macaques performing a pair-association memory task. Cortical layers were estimated on the basis of current source density profiles with histological verifications, and the interlaminar signal flow was determined with cross-correlation analysis between spike trains. During the cue period, canonical "feed-forward" signals flowed from granular to supragranular layers and from supragranular to infragranular layers. During the delay period, however, the signal flow reversed to the "feed-back" direction: from infragranular to supragranular layers. This reversal of signal flow highlights how the temporal cortex differentially recruits its laminar circuits for sensory and mnemonic processing.     

Visual receptive fields of neurons in inferotemporal cortex of the monkey

Neurons in inferotemporal cortex (area TE) of the monkey had visual receptive fields which were very large (greater than 10 by 10 degrees) and almost always included the fovea. Some extended well into both halves of the visual field, while others were confined to the ipsilateral or contralateral side. These neurons were differentially sensitive to several of the following dimensions of the stimulus: size and shape, color, orientation, and direction of movement.     

How visual stimuli activate dopaminergic neurons at short latency

Unexpected, biologically salient stimuli elicit a short-latency, phasic response in midbrain dopaminergic (DA) neurons. Although this signal is important for reinforcement learning, the information it conveys to forebrain target structures remains uncertain. One way to decode the phasic DA signal would be to determine the perceptual properties of sensory inputs to DA neurons. After local disinhibition of the superior colliculus in anesthetized rats, DA neurons became visually responsive, whereas disinhibition of the visual cortex was ineffective. As the primary source of visual afferents, the limited processing capacities of the colliculus may constrain the visual information content of phasic DA responses.     

Neural mechanisms of visual attention: how top-down feedback highlights relevant locations

Attention helps us process potentially important objects by selectively increasing the activity of sensory neurons that represent the relevant locations and features of our environment. This selection process requires top-down feedback about what is important in our environment. We investigated how parietal cortical output influences neural activity in early sensory areas. Neural recordings were made simultaneously from the posterior parietal cortex and an earlier area in the visual pathway, the medial temporal area, of macaques performing a visual matching task. When the monkey selectively attended to a location, the timing of activities in the two regions became synchronized, with the parietal cortex leading the medial temporal area. Parietal neurons may thus selectively increase activity in earlier sensory areas to enable focused spatial attention.     

Auditory association cortex lesions impair auditory short-term memory in monkeys

Monkeys that were trained to perform auditory and visual short-term memory tasks (delayed matching-to-sample) received lesions of the auditory association cortex in the superior temporal gyrus. Although visual memory was completely unaffected by the lesions, auditory memory was severely impaired. Despite this impairment, all monkeys could discriminate sounds closer in frequency than those used in the auditory memory task. This result suggests that the superior temporal cortex plays a role in auditory processing and retention similar to the role the inferior temporal cortex plays in visual processing and retention.     

Neuroscience. More to seeing than meets the eye

A single event may elicit several different sensory stimuli such as vision, sound, and touch. But how does the brain know which of the many different stimuli arriving in the sensory cortex of the brain are connected? In her Perspective, de Gelder discusses new findings showing that when a touch is applied on the same side of the body as a visual cue, vision is enhanced (Macaluso et al.). She explains that this effect is due to neurons projecting from the somatosensory (touch) area of the sensory cortex back to the visual cortex. These neurons keep the visual cortex informed about tactile stimuli elicited at the same time as the visual stimuli.     

Selectivity for 3D shape that reveals distinct areas within macaque inferior temporal cortex

The anterior part of the macaque inferior temporal cortex, area TE, occupies a large portion of the temporal lobe and is critical for object recognition. Thus far, no relation between anatomical subdivisions of TE and neuronal selectivity has been described. Here, we present evidence that neurons selective for three-dimensional (3D) shape are concentrated in the lower bank of the superior temporal sulcus, whereas neurons in lateral TE are generally unselective for 3D shape, though equally selective for 2D shape. These findings reveal that TE consists of at least two distinct areas, one of which processes a specific object property.     

Sparse coding and decorrelation in primary visual cortex during natural vision

Theoretical studies suggest that primary visual cortex (area V1) uses a sparse code to efficiently represent natural scenes. This issue was investigated by recording from V1 neurons in awake behaving macaques during both free viewing of natural scenes and conditions simulating natural vision. Stimulation of the nonclassical receptive field increases the selectivity and sparseness of individual V1 neurons, increases the sparseness of the population response distribution, and strongly decorrelates the responses of neuron pairs. These effects are due to both excitatory and suppressive modulation of the classical receptive field by the nonclassical receptive field and do not depend critically on the spatiotemporal structure of the stimuli. During natural vision, the classical and nonclassical receptive fields function together to form a sparse representation of the visual world. This sparse code may be computationally efficient for both early vision and higher visual processing.     

Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex

Astrocytes have long been thought to act as a support network for neurons, with little role in information representation or processing. We used two-photon imaging of calcium signals in the ferret visual cortex in vivo to discover that astrocytes, like neurons, respond to visual stimuli, with distinct spatial receptive fields and sharp tuning to visual stimulus features including orientation and spatial frequency. The stimulus-feature preferences of astrocytes were exquisitely mapped across the cortical surface, in close register with neuronal maps. The spatially restricted stimulus-specific component of the intrinsic hemodynamic mapping signal was highly sensitive to astrocyte activation, indicating that astrocytes have a key role in coupling neuronal organization to mapping signals critical for noninvasive brain imaging. Furthermore, blocking astrocyte glutamate transporters influenced the magnitude and duration of adjacent visually driven neuronal responses.     

The role of working memory in visual selective attention

The hypothesis that working memory is crucial for reducing distraction by maintaining the prioritization of relevant information was tested in neuroimaging and psychological experiments with humans. Participants performed a selective attention task that required them to ignore distractor faces while holding in working memory a sequence of digits that were in the same order (low memory load) or a different order (high memory load) on every trial. Higher memory load, associated with increased prefrontal activity, resulted in greater interference effects on behavioral performance from the distractor faces, plus increased face-related activity in the visual cortex. These findings confirm a major role for working memory in the control of visual selective attention.     

Fast-forward playback of recent memory sequences in prefrontal cortex during sleep

As previously shown in the hippocampus and other brain areas, patterns of firing-rate correlations between neurons in the rat medial prefrontal cortex during a repetitive sequence task were preserved during subsequent sleep, suggesting that waking patterns are reactivated. We found that, during sleep, reactivation of spatiotemporal patterns was coherent across the network and compressed in time by a factor of 6 to 7. Thus, when behavioral constraints are removed, the brain's intrinsic processing speed may be much faster than it is in real time. Given recent evidence implicating the medial prefrontal cortex in retrieval of long-term memories, the observed replay may play a role in the process of memory consolidation.     

Long-term potentiation in the motor cortex

Long-term potentiation (LTP) is a model for learning and memory processes. Tetanic stimulation of the sensory cortex produces LTP in motor cortical neurons, whereas tetanization of the ventrolateral nucleus of the thalamus, which also projects to the motor cortex, does not. However, after simultaneous high-frequency stimulation of both the sensory cortex and the ventrolateral nucleus of the thalamus, LTP of thalamic input to motor cortical neurons is induced. This associative LTP occurs only in neurons in the superficial layers of the motor cortex that receive monosynaptic input from both the sensory cortex and the ventrolateral nucleus of the thalamus. Associative LTP in the motor cortex may constitute a basis for the retention of motor skills.     

Selective attention gates visual processing in the extrastriate cortex

Single cells were recorded in the visual cortex of monkeys trained to attend to stimuli at one location in the visual field and ignore stimuli at another. When both locations were within the receptive field of a cell in prestriate area V4 or the inferior temporal cortex, the response to the unattended stimulus was dramatically reduced. Cells in the striate cortex were unaffected by attention. The filtering of irrelevant information from the receptive fields of extrastriate neurons may underlie the ability to identify and remember the properties of a particular object out of the many that may be represented on the retina.     

Two functional channels from primary visual cortex to dorsal visual cortical areas

Relationships between the M and P retino-geniculo-cortical visual pathways and "dorsal" visual areas were investigated by measuring the sources of local excitatory input to individual neurons in layer 4B of primary visual cortex. We found that contributions of the M and P pathways to layer 4B neurons are dependent on cell type. Spiny stellate neurons receive strong M input through layer 4Calpha and no significant P input through layer 4Cbeta. In contrast, pyramidal neurons in layer 4B receive strong input from both layers 4Calpha and 4Cbeta. These observations, along with evidence that direct input from layer 4B to area MT arises predominantly from spiny stellates, suggest that these different cell types constitute two functionally specialized subsystems.     

Neuroscience. Noise makes sense in neuronal computing

The united efforts of assemblies of neurons in the brain's primary visual cortex translate incoming visual signals into action potentials. These action potentials encode, for example, the contrast and orientation of different parts of the image. Some neurons are sensitive to one particular orientation, other are sensitive to other orientations, but all neurons respond equally well to the image contrast. In a Perspective, Volgushev and Eysel explain the finding (Anderson et al.) that neurons are able to maintain this sensitivity to the orientation of a stimulus regardless of the contrast by adding noise to the membrane potential, such that action potentials can also be generated in response to weak signals at low contrast.     

Reward timing in the primary visual cortex

We discovered that when adult rats experience an association between visual stimuli and subsequent rewards, the responses of a substantial fraction of neurons in the primary visual cortex evolve from those that relate solely to the physical attributes of the stimuli to those that accurately predict the timing of reward. In addition to revealing a remarkable type of response plasticity in adult V1, these data demonstrate that reward-timing activity-a "higher" brain function-can occur very early in sensory-processing paths. These findings challenge the traditional interpretation of activity in the primary visual cortex.     

Internally generated reactivation of single neurons in human hippocampus during free recall

The emergence of memory, a trace of things past, into human consciousness is one of the greatest mysteries of the human mind. Whereas the neuronal basis of recognition memory can be probed experimentally in human and nonhuman primates, the study of free recall requires that the mind declare the occurrence of a recalled memory (an event intrinsic to the organism and invisible to an observer). Here, we report the activity of single neurons in the human hippocampus and surrounding areas when subjects first view cinematic episodes consisting of audiovisual sequences and again later when they freely recall these episodes. A subset of these neurons exhibited selective firing, which often persisted throughout and following specific episodes for as long as 12 seconds. Verbal reports of memories of these specific episodes at the time of free recall were preceded by selective reactivation of the same hippocampal and entorhinal cortex neurons. We suggest that this reactivation is an internally generated neuronal correlate for the subjective experience of spontaneous emergence of human recollection.     

Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex

Monocular deprivation during early postnatal development remodels the circuitry of the primary visual cortex so that most neurons respond poorly to stimuli presented to the deprived eye. This rapid physiological change is ultimately accompanied by a matching anatomical loss of input from the deprived eye. This remodeling is thought to be initiated at the thalamocortical synapse. Ocular dominance plasticity after brief (24 hours) monocular deprivation was analyzed by intrinsic signal optical imaging and by targeted extracellular unit recordings. Deprived-eye responsiveness was lost in the extragranular layers, whereas normal binocularity in layer IV was preserved. This finding supports the hypothesis that thalamocortical organization is guided by earlier changes at higher stages.