Neuronal correlate of pictorial short-term memory in the primate temporal cortex

It has been proposed that visual-memory traces are located in the temporal lobes of the cerebral cortex, as electric stimulation of this area in humans results in recall of imagery. Lesions in this area also affect recognition of an object after a delay in both humans and monkeys, indicating a role in short-term memory of images. Single-unit recordings from the temporal cortex have shown that some neurons continue to fire when one of two or four colours are to be remembered temporarily. But neuronal responses selective to specific complex objects, including hands and faces, cease soon after the offset of stimulus presentation. These results led to the question of whether any of these neurons could serve the memory of complex objects. We report here a group of shape-selective neurons in an anterior ventral part of the temporal cortex of monkeys that exhibited sustained activity during the delay period of a visual short-term memory task. The activity was highly selective for the pictorial information to be memorized and was independent of the physical attributes such as size, orientation, colour or position of the object. These observations show that the delay activity represents the short-term memory of the categorized percept of a picture.     

Visual categorization shapes feature selectivity in the primate temporal cortex.

The way that we perceive and interact with objects depends on our previous experience with them. For example, a bird expert is more likely to recognize a bird as a sparrow, a sandpiper or a cockatiel than a non-expert. Neurons in the inferior temporal cortex have been shown to be important in the representation of visual objects; however, it is unknown which object features are represented and how these representations are affected by categorization training. Here we show that feature selectivity in the macaque inferior temporal cortex is shaped by categorization of objects on the basis of their visual features. Specifically, we recorded from single neurons while monkeys performed a categorization task with two sets of parametric stimuli. Each stimulus set consisted of four varying features, but only two of the four were important for the categorization task (diagnostic features). We found enhanced neuronal representation of the diagnostic features relative to the non-diagnostic ones. These findings demonstrate that stimulus features important for categorization are instantiated in the activity of single units (neurons) in the primate inferior temporal cortex.     

Neuronal correlates of parametric working memory in the prefrontal cortex.

Humans and monkeys have similar abilities to discriminate the difference in frequency between two mechanical vibrations applied sequentially to the fingertips. A key component of this sensory task is that the second stimulus is compared with the trace left by the first (base) stimulus, which must involve working memory. Where and how is this trace held in the brain? This question was investigated by recording from single neurons in the prefrontal cortex of monkeys while they performed the somatosensory discrimination task. Here we describe neurons in the inferior convexity of the prefrontal cortex whose discharge rates varied, during the delay period between the two stimuli, as a monotonic function of the base stimulus frequency. We describe this as 'monotonic stimulus encoding', and we suggest that the result may generalize: monotonic stimulus encoding may be the basic representation of one-dimensional sensory stimulus quantities in working memory. Thus we predict that other behavioural tasks that require ordinal comparisons between scalar analogue stimuli would give rise to monotonic responses similar to those reported here.     

An unexpected specialization for horizontal disparity in primate primary visual cortex

The horizontal separation of the eyes means that objects nearer or farther than the fixation point project to different locations on the two retinae, differing principally in their horizontal coordinates (horizontal binocular disparity). Disparity-selective neurons have generally been studied with disparities applied in only one direction (often horizontal), which cannot determine whether the encoding is specialized for processing disparities along the horizontal axis. It is therefore unclear if disparity selectivity represents a specialization for naturally occurring disparities. I used random dot stereograms to study disparity-selective neurons from the primary visual cortex (V1) of awake fixating monkeys. Many combinations of vertical and horizontal disparity were used, characterizing the surface of responses as a function of two-dimensional disparity. Here I report that the response surface usually showed elongation along the horizontal disparity axis, despite the isotropic stimulus. Thus these neurons modulated their firing rate over a wider range of horizontal disparity than vertical disparity. This demonstrates that disparity-selective cells are specialized for processing horizontal disparity, and that existing models of disparity selectivity require substantial revision.     

Calbindin immunoreactivity alternates with cytochrome c-oxidase-rich zones in some layers of the primate visual cortex

Calcium ions have a pivotal role in many neuronal activities, but little is known about their involvement in the cortical processing of visual information. Using immunohistochemical methods, we have now detected a calcium-binding protein, calbindin-D-28K, which may confer on certain compartments of cortical area 17 the ability to modulate Ca2+ metabolism. Thus, calbindin occurs in the primate striate cortex in a pattern almost complementary to that displaying strong cytochrome c-oxidase activity. From this and other observations, we deduce that the distribution of calbindin-immunoreactive sites corresponds mainly to extra-geniculocortical connections of the primary visual cortex. This implies that the geniculocortical and extra-geniculocortical compartments of area 17 differ in an intracellular system for Ca2+ homeostasis.     

Segregation of global and local motion processing in primate middle temporal visual area.

The early stages of primate visual processing appear to be divided up into several component parts so that, for example, colour, form and motion are analysed by anatomically distinct streams. We have found that further subspecialization occurs within the motion processing stream. Neurons representing two different kinds of information about visual motion are segregated in columnar fashion within the middle temporal area of the owl monkey. These columns can be distinguished by labelling with 2-deoxyglucose in response to large-field random-dot patterns. Neurons in lightly labelled interbands have receptive fields with antagonistic surrounds: the response to a centrally placed moving stimulus is suppressed by motion in the surround. Neurons in more densely labelled bands have surrounds that reinforce the centre response so that they integrate motion cues over large areas of the visual field. Interband cells carry information about local motion contrast that may be used to detect motion boundaries or to indicate retinal slip during visual tracking. Band cells encode information about global motion that might be useful for orienting the animal in its environment.     

Capacity limit of visual short-term memory in human posterior parietal cortex

At any instant, our visual system allows us to perceive a rich and detailed visual world. Yet our internal, explicit representation of this visual world is extremely sparse: we can only hold in mind a minute fraction of the visual scene. These mental representations are stored in visual short-term memory (VSTM). Even though VSTM is essential for the execution of a wide array of perceptual and cognitive functions, and is supported by an extensive network of brain regions, its storage capacity is severely limited. With the use of functional magnetic resonance imaging, we show here that this capacity limit is neurally reflected in one node of this network: activity in the posterior parietal cortex is tightly correlated with the limited amount of scene information that can be stored in VSTM. These results suggest that the posterior parietal cortex is a key neural locus of our impoverished mental representation of the visual world.     

Global and fine information coded by single neurons in the temporal visual cortex.

When we see a person's face, we can easily recognize their species, individual identity and emotional state. How does the brain represent such complex information? A substantial number of neurons in the macaque temporal cortex respond to faces. However, the neuronal mechanisms underlying the processing of complex information are not yet clear. Here we recorded the activity of single neurons in the temporal cortex of macaque monkeys while presenting visual stimuli consisting of geometric shapes, and monkey and human faces with various expressions. Information theory was used to investigate how well the neuronal responses could categorize the stimuli. We found that single neurons conveyed two different scales of facial information in their firing patterns, starting at different latencies. Global information, categorizing stimuli as monkey faces, human faces or shapes, was conveyed in the earliest part of the responses. Fine information about identity or expression was conveyed later, beginning on average 51 ms after global information. We speculate that global information could be used as a 'header' to prepare destination areas for receiving more detailed information.     

Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex

In the hippocampus and neocortex, high-frequency (tetanic) stimulation of an afferent pathway leads to long-term potentiation (LTP) of synaptic transmission. In the hippocampus it has recently been shown that long-term depression (LTD) of excitatory transmission can also be induced by certain combinations of synaptic activation. In most hippocampal and all neocortical pathways studied so far, the induction of LTP requires the activation of N-methyl-D-aspartate (NMDA) receptor-gated conductances. Here we report that LTD can occur in neurons of slices of the rat visual cortex and that the same tetanic stimulation can induce either LTP or LTD depending on the level of depolarization of the postsynaptic neuron. By applying intracellular current injections or pharmacological disinhibition to modify the depolarizing response of the postsynaptic neuron to tetanic stimulation, we show that the mechanisms of induction of LTD and LTP are both postsynaptic. LTD is obtained if postsynaptic depolarization exceeds a critical level but remains below a threshold related to NMDA receptor-gated conductances, whereas LTP is induced if this second threshold is reached.     

Relative reward preference in primate orbitofrontal cortex

The orbital part of prefrontal cortex appears to be crucially involved in the motivational control of goal-directed behaviour. Patients with lesions of orbitofrontal cortex show impairments in making decisions about the expected outcome of actions. Monkeys with orbitofrontal lesions respond abnormally to changes in reward expectations and show altered reward preferences. As rewards constitute basic goals of behaviour, we investigated here how neurons in the orbitofrontal cortex of monkeys process information about liquid and food rewards in a typical frontal task, spatial delayed responding. The activity of orbitofrontal neurons increases in response to reward-predicting signals, during the expectation of rewards, and after the receipt of rewards. Neurons discriminate between different rewards, mainly irrespective of the spatial and visual features of reward-predicting stimuli and behavioural reactions. Most reward discriminations reflect the animals' relative preference among the available rewards, as expressed by their choice behaviour, rather than physical reward properties. Thus, neurons in the orbitofrontal cortex appear to process the motivational value of rewarding outcomes of voluntary action.     

A disinhibitory microcircuit for associative fear learning in the auditory cortex

Learning causes a change in how information is processed by neuronal circuits. Whereas synaptic plasticity, an important cellular mechanism, has been studied in great detail, we know much less about how learning is implemented at the level of neuronal circuits and, in particular, how interactions between distinct types of neurons within local networks contribute to the process of learning. Here we show that acquisition of associative fear memories depends on the recruitment of a disinhibitory microcircuit in the mouse auditory cortex. Fear-conditioning-associated disinhibition in auditory cortex is driven by foot-shock-mediated cholinergic activation of layer 1 interneurons, in turn generating inhibition of layer 2/3 parvalbumin-positive interneurons. Importantly, pharmacological or optogenetic block of pyramidal neuron disinhibition abolishes fear learning. Together, these data demonstrate that stimulus convergence in the auditory cortex is necessary for associative fear learning to complex tones, define the circuit elements mediating this convergence and suggest that layer-1-mediated disinhibition is an important mechanism underlying learning and information processing in neocortical circuits.     

The neuronal representation of pitch in primate auditory cortex

Pitch perception is critical for identifying and segregating auditory objects, especially in the context of music and speech. The perception of pitch is not unique to humans and has been experimentally demonstrated in several animal species. Pitch is the subjective attribute of a sound's fundamental frequency (f(0)) that is determined by both the temporal regularity and average repetition rate of its acoustic waveform. Spectrally dissimilar sounds can have the same pitch if they share a common f(0). Even when the acoustic energy at f(0) is removed ('missing fundamental') the same pitch is still perceived. Despite its importance for hearing, how pitch is represented in the cerebral cortex is unknown. Here we show the existence of neurons in the auditory cortex of marmoset monkeys that respond to both pure tones and missing fundamental harmonic complex sounds with the same f(0), providing a neural correlate for pitch constancy. These pitch-selective neurons are located in a restricted low-frequency cortical region near the anterolateral border of the primary auditory cortex, and is consistent with the location of a pitch-selective area identified in recent imaging studies in humans.     

Neuronal basis of age-related working memory decline

Many of the cognitive deficits of normal ageing (forgetfulness, distractibility, inflexibility and impaired executive functions) involve prefrontal cortex (PFC) dysfunction. The PFC guides behaviour and thought using working memory, which are essential functions in the information age. Many PFC neurons hold information in working memory through excitatory networks that can maintain persistent neuronal firing in the absence of external stimulation. This fragile process is highly dependent on the neurochemical environment. For example, elevated cyclic-AMP signalling reduces persistent firing by opening HCN and KCNQ potassium channels. It is not known if molecular changes associated with normal ageing alter the physiological properties of PFC neurons during working memory, as there have been no in vivo recordings, to our knowledge, from PFC neurons of aged monkeys. Here we characterize the first recordings of this kind, revealing a marked loss of PFC persistent firing with advancing age that can be rescued by restoring an optimal neurochemical environment. Recordings showed an age-related decline in the firing rate of DELAY neurons, whereas the firing of CUE neurons remained unchanged with age. The memory-related firing of aged DELAY neurons was partially restored to more youthful levels by inhibiting cAMP signalling, or by blocking HCN or KCNQ channels. These findings reveal the cellular basis of age-related cognitive decline in dorsolateral PFC, and demonstrate that physiological integrity can be rescued by addressing the molecular needs of PFC circuits.     

Neuronal properties underlying processing of visual information in the barnacle.

Generation of a transient, amplified response to the dimming of light in the visual system of the barnacle involves two synaptic stages. It is accomplished primarily by decrementally conducting neurones that are similar to bipolar cells of the vertebrate retina.     

Neuronal synchrony does not correlate with motion coherence in cortical area MT

Natural visual scenes are cluttered with multiple objects whose individual features must somehow be selectively linked (or 'bound') if perception is to coincide with reality. Recent neurophysiological evidence supports a 'binding-by-synchrony' hypothesis: neurons excited by features of the same object fire synchronously, while neurons excited by features of different objects do not. Moving plaid patterns offer a straightforward means to test this idea. By appropriate manipulations of apparent transparency, the component gratings of a plaid pattern can be seen as parts of a single coherently moving surface or as two non-coherently moving surfaces. We examined directional tuning and synchrony of area-MT neurons in awake, fixating primates in response to perceptually coherent and non-coherent plaid patterns. Here we show that directional tuning correlated highly with perceptual coherence, which is consistent with an earlier study. Although we found stimulus-dependent synchrony, coherent plaids elicited significantly less synchrony than did non-coherent plaids. Our data therefore do not support the binding-by-synchrony hypothesis as applied to this class of motion stimuli in area MT.     

Attention modulates synchronized neuronal firing in primate somatosensory cortex

A potentially powerful information processing strategy in the brain is to take advantage of the temporal structure of neuronal spike trains. An increase in synchrony within the neural representation of an object or location increases the efficacy of that neural representation at the next synaptic stage in the brain; thus, increasing synchrony is a candidate for the neural correlate of attentional selection. We investigated the synchronous firing of pairs of neurons in the secondary somatosensory cortex (SII) of three monkeys trained to switch attention between a visual task and a tactile discrimination task. We found that most neuron pairs in SII cortex fired synchronously and, furthermore, that the degree of synchrony was affected by the monkey's attentional state. In the monkey performing the most difficult task, 35% of neuron pairs that fired synchronously changed their degree of synchrony when the monkey switched attention between the tactile and visual tasks. Synchrony increased in 80% and decreased in 20% of neuron pairs affected by attention.