Who is that? Brain networks and mechanisms for identifying individuals

Social animals can identify conspecifics by many forms of sensory input. However, whether the neuronal computations that support this ability to identify individuals rely on modality-independent convergence or involve ongoing synergistic interactions along the multiple sensory streams remains controversial. Direct neuronal measurements at relevant brain sites could address such questions, but this requires better bridging the work in humans and animal models. Here, we overview recent studies in nonhuman primates on voice and face identity-sensitive pathways and evaluate the correspondences to relevant findings in humans. This synthesis provides insights into converging sensory streams in the primate anterior temporal lobe (ATL) for identity processing. Furthermore, we advance a model and suggest how alternative neuronal mechanisms could be tested

Latency and Selectivity of Single Neurons Indicate Hierarchical Processing in the Human Medial Temporal Lobe

Neurons in the temporal lobe of both monkeys and humans show selective responses to classes of visual stimuli and even to specific individuals. In this study, we investigate the latency and selectivity of visually responsive neurons recorded from microelectrodes in the parahippocampal cortex, entorhinal cortex, hippocampus, and amygdala of human subjects during a visual object presentation task. During 96 experimental sessions in 35 subjects, we recorded from a total of 3278 neurons. Of these units, 398 responded selectively to one or more of the presented stimuli. Mean response latencies were substantially larger than those reported in monkeys. We observed a highly significant correlation between the latency and the selectivity of these neurons: the longer the latency the greater the selectivity. Particularly, parahippocampal neurons were found to respond significantly earlier and less selectively than those in the other three regions. Regional analysis showed significant correlations between latency and selectivity within the parahippocampal cortex, entorhinal cortex, and hippocampus, but not within the amygdala. The later and more selective responses tended to be generated by cells with sparse baseline firing rates and vice versa. Our results provide direct evidence for hierarchical processing of sensory information at the interface between the visual pathway and the limbic system, by which increasingly refined and specific representations of stimulus identity are generated over time along the anatomic pathways of the medial temporal lobe

Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex

The integration of auditory and visual stimuli is crucial for recognizing objects, communicating effectively, and navigating through our complex world. Although the frontal lobes are involved in memory, communication, and language, there has been no evidence that the integration of communication information occurs at the single-cell level in the frontal lobes. Here, we show that neurons in the macaque ventrolateral prefrontal cortex (VLPFC) integrate audiovisual communication stimuli. The multisensory interactions included both enhancement and suppression of a predominantly auditory or a predominantly visual response, although multisensory suppression was the more common mode of response. The multisensory neurons were distributed across the VLPFC and within previously identified unimodal auditory and visual regions (O’Scalaidhe et al., 1997; Romanski and Goldman-Rakic, 2002). Thus, our study demonstrates, for the first time, that single prefrontal neurons integrate communication information from the auditory and visual domains, suggesting that these neurons are an important node in the cortical network responsible for communication

Neural population coding: combining insights from microscopic and mass signals

Behavior relies on the distributed and coordinated activity of neural populations. Population activity can be measured using multi-neuron recordings and neuroimaging. Neural recordings reveal how the heterogeneity, sparseness, timing, and correlation of population activity shape information processing in local networks, whereas neuroimaging shows how long-range coupling and brain states impact on local activity and perception. To obtain an integrated perspective on neural information processing we need to combine knowledge from both levels of investigation. We review recent progress of how neural recordings, neuroimaging, and computational approaches begin to elucidate how interactions between local neural population activity and large-scale dynamics shape the structure and coding capacity of local information representations, make them state-dependent, and control distributed populations that collectively shape behavior

Independent coding of absolute duration and distance magnitudes in the prefrontal cortex

The estimation of space and time can interfere with each other, and neuroimaging studies have shown overlapping activation in the parietal and prefrontal cortical areas. We used duration and distance discrimination tasks to determine whether space and time share resources in prefrontal cortex (PF) neurons. Monkeys were required to report which of two stimuli, a red circle or blue square, presented sequentially, were longer and farther, respectively, in the duration and distance tasks. In a previous study, we showed that relative duration and distance are coded by different populations of neurons and that the only common representation is related to goal coding. Here, we examined the coding of absolute duration and distance. Our results support a model of independent coding of absolute duration and distance metrics by demonstrating that not only relative magnitude but also absolute magnitude are independently coded in the PF

The cognitive neuroscience of visual working memory

Visual working memory allows us to temporarily maintain and manipulate visual information in order to solve a task. The study of the brain mechanisms underlying this function began more than half a century ago, with Scoville and Milner’s (1957) seminal discoveries with amnesic patients. This timely collection of papers brings together diverse perspectives on the cognitive neuroscience of visual working memory from multiple fields that have traditionally been fairly disjointed: human neuroimaging, electrophysiological, behavioural and animal lesion studies, investigating both the developing and the adult brain

Information Theory’s failure in neuroscience: on the limitations of cybernetics

In Cybernetics (1961 Edition), Professor Norbert Wiener noted that “The role of information and the technique of measuring and transmitting information constitute a whole discipline for the engineer, for the neuroscientist, for the psychologist, and for the sociologist”. Sociology aside, the neuroscientists and the psychologists inferred “information transmitted” using the discrete summations from Shannon Information Theory. The present author has since scrutinized the psychologists’ approach in depth, and found it wrong. The neuroscientists’ approach is highly related, but remains unexamined. Neuroscientists quantified “the ability of [physiological sensory] receptors (or other signal-processing elements) to transmit information about stimulus parameters”. Such parameters could vary along a single continuum (e.g., intensity), or along multiple dimensions that altogether provide a Gestalt – such as a face. Here, unprecedented scrutiny is given to how 23 neuroscience papers computed “information transmitted” in terms of stimulus parameters and the evoked neuronal spikes. The computations relied upon Shannon’s “confusion matrix”, which quantifies the fidelity of a “general communication system”. Shannon’s matrix is square, with the same labels for columns and for rows. Nonetheless, neuroscientists labelled the columns by “stimulus category” and the rows by “spike-count category”. The resulting “information transmitted” is spurious, unless the evoked spike-counts are worked backwards to infer the hypothetical evoking stimuli. The latter task is probabilistic and, regardless, requires that the confusion matrix be square. Was it? For these 23 significant papers, the answer is No

The contribution of fMRI in the study of visual categorization and expertise

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Homunculus strides again: why ‘information transmitted’ in neuroscience tells us nothing

Purpose – For half a century, neuroscientists have used Shannon Information Theory to calculate “information transmitted,” a hypothetical measure of how well neurons “discriminate” amongst stimuli. Neuroscientists’ computations, however, fail to meet even the technical requirements for credibility. Ultimately, the reasons must be conceptual. That conclusion is confirmed here, with crucial implications for neuroscience. The paper aims to discuss these issues. Design/methodology/approach – Shannon Information Theory depends upon a physical model, Shannon’s “general communication system.” Neuroscientists’ interpretation of that model is scrutinized here. Findings – In Shannon’s system, a recipient receives a message composed of symbols. The symbols received, the symbols sent, and their hypothetical occurrence probabilities altogether allow calculation of “information transmitted.” Significantly, Shannon’s system’s “reception” (decoding) side physically mirrors its “transmission” (encoding) side. However, neurons lack the “reception” side; neuroscientists nonetheless insisted that decoding must happen. They turned to Homunculus, an internal humanoid who infers stimuli from neuronal firing. However, Homunculus must contain a Homunculus, and so on ad infinitum – unless it is super-human. But any need for Homunculi, as in “theories of consciousness,” is obviated if consciousness proves to be “emergent.” Research limitations/implications – Neuroscientists’ “information transmitted” indicates, at best, how well neuroscientists themselves can use neuronal firing to discriminate amongst the stimuli given to the research animal. Originality/value – A long-overdue examination unmasks a hidden element in neuroscientists’ use of Shannon Information Theory, namely, Homunculus. Almost 50 years’ worth of computations are recognized as irrelevant, mandating fresh approaches to understanding “discriminability.

Occlusion-related lateral connections stabilize kinetic depth stimuli through perceptual coupling

Local sensory information is often ambiguous forcing the brain to integrate spatiotemporally separated information for stable conscious perception. Lateral connections between clusters of similarly tuned neurons in the visual cortex are a potential neural substrate for the coupling of spatially separated visual information. Ecological optics suggests that perceptual coupling of visual information is particularly beneficial in occlusion situations. Here we present a novel neural network model and a series of human psychophysical experiments that can together explain the perceptual coupling of kinetic depth stimuli with activity-driven lateral information sharing in the far depth plane. Our most striking finding is the perceptual coupling of an ambiguous kinetic depth cylinder with a coaxially presented and disparity defined cylinder backside, while a similar frontside fails to evoke coupling. Altogether, our findings are consistent with the idea that clusters of similarly tuned far depth neurons share spatially separated motion information in order to resolve local perceptual ambiguities. The classification of far depth in the facilitation mechanism results from a combination of absolute and relative depth that suggests a functional role of these lateral connections in the perception of partially occluded objects