Mariano Sigman

The Neural Basis of Perceptual Learning

Perceptual learning is a lifelong process. We begin by encoding information about the basic structure of the natural world and continue to assimilate information about specific patterns with which we become familiar. The specificity of the learning suggests that all areas of the cerebral cortex are plastic and can represent various aspects of learned information. The neural substrate of perceptual learning relates to the nature of the neural code itself, including changes in cortical maps, in the temporal characteristics of neuronal responses, and in modulation of contextual influences. Top-down control of these representations suggests that learning involves an interaction between multiple cortical areas.

Brain States: Top-Down Influences in Sensory Processing

All cortical and thalamic levels of sensory processing are subject to powerful top-down influences, the shaping of lower-level processes by more complex information. New findings on the diversity of top-down interactions show that cortical areas function as adaptive processors, being subject to attention, expectation, and perceptual task. Brain states are determined by the interactions between multiple cortical areas and the modulation of intrinsic circuits by feedback connections. In perceptual learning, both the encoding and recall of learned information involves a selection of the appropriate inputs that convey information about the stimulus being discriminated. Disruption of this interaction may lead to behavioral disorders, including schizophrenia.

Hierarchical coding of letter strings in the ventral stream: Dissecting the inner organization of the visual word-form system

Visual word recognition has been proposed to rely on a hierarchy of increasingly complex neuronal detectors, from individual letters to bigrams and morphemes. We used fMRI to test whether such a hierarchy is present in the left occipitotemporal cortex, at the site of the visual word-form area, and with an anterior-to-posterior progression. We exposed adult readers to (1) false-font strings; (2) strings of infrequent letters; (3) strings of frequent letters but rare bigrams; (4) strings with frequent bigrams but rare quadrigrams; (5) strings with frequent quadrigrams; (6) real words. A gradient of selectivity was observed through the entire span of the occipitotemporal cortex, with activation becoming more selective for higher-level stimuli toward the anterior fusiform region. A similar gradient was also seen in left inferior frontoinsular cortex. Those gradients were asymmetrical in favor of the left hemisphere. We conclude that the left occipitotemporal visual word-form area, far from being a homogeneous structure, presents a high degree of functional and spatial hierarchical organization which must result from a tuning process during reading acquisition.

On a common circle: Natural scenes and Gestalt rules

To understand how the human visual system analyzes images, it is essential to know the structure of the visual environment. In particular, natural images display consistent statistical properties that distinguish them from random luminance distributions. We have studied the geometric regularities of oriented elements (edges or line segments) present in an ensemble of visual scenes, asking how much information the presence of a segment in a particular location of the visual scene carries about the presence of a second segment at different relative positions and orientations. We observed strong long-range correlations in the distribution of oriented segments that extend over the whole visual field. We further show that a very simple geometric rule, cocircularity, predicts the arrangement of segments in natural scenes, and that different geometrical arrangements show relevant differences in their scaling properties. Our results show similarities to geometric features of previous physiological and psychophysical studies. We discuss the implications of these findings for theories of early vision.

Functional organization of perisylvian activation during presentation of sentences in preverbal infants

We examined the functional organization of cerebral activity in 3-month-old infants when they were listening to their mother language. Short sentences were presented in a slow event-related functional MRI paradigm. We then parsed the infants network of perisylvian responsive regions into functionally distinct regions based on their speed of activation and sensitivity to sentence repetition. An adult-like structure of functional MRI response delays was observed along the superior temporal regions, suggesting a hierarchical processing scheme. The fastest responses were recorded in the vicinity of Heschls gyrus, whereas responses became increasingly slower toward the posterior part of the superior temporal gyrus and toward the temporal poles and inferior frontal regions (Brocas area). Activation in the latter region increased when the sentence was repeated after a 14-s delay, suggesting the early involvement of Brocas area in verbal memory. The fact that Brocas area is active in infants before the babbling stage implies that activity in this region is not the consequence of sophisticated motor learning but, on the contrary, that this region may drive, through interactions with the perceptual system, the learning of the complex motor sequences required for future speech production. Our results point to a complex, hierarchical organization of the human brain in the first months of life, which may play a crucial role in language acquisition in our species.

Signature of consciousness in the dynamics of resting-state brain activity

Significance What are the origins of resting-state functional connectivity patterns? One dominating view is that they index ongoing cognitive processes. However, this conclusion is in conflict with studies showing that long-range functional connectivity persists after loss of consciousness, possibly reflecting structural connectivity maps. In this work we respond to this question showing that in fact both sources have a clear and separable contribution to resting-state patterns. We show that under anesthesia, the dominating functional configurations have low information capacity and lack negative correlations. Importantly, they are rigid, tied to the anatomical map. Conversely, wakefulness is characterized by the dynamical exploration of a rich, flexible repertoire of functional configurations. These dynamical properties constitute a signature of consciousness. At rest, the brain is traversed by spontaneous functional connectivity patterns. Two hypotheses have been proposed for their origins: they may reflect a continuous stream of ongoing cognitive processes as well as random fluctuations shaped by a fixed anatomical connectivity matrix. Here we show that both sources contribute to the shaping of resting-state networks, yet with distinct contributions during consciousness and anesthesia. We measured dynamical functional connectivity with functional MRI during the resting state in awake and anesthetized monkeys. Under anesthesia, the more frequent functional connectivity patterns inherit the structure of anatomical connectivity, exhibit fewer small-world properties, and lack negative correlations. Conversely, wakefulness is characterized by the sequential exploration of a richer repertoire of functional configurations, often dissimilar to anatomical structure, and comprising positive and negative correlations among brain regions. These results reconcile theories of consciousness with observations of long-range correlation in the anesthetized brain and show that a rich functional dynamics might constitute a signature of consciousness, with potential clinical implications for the detection of awareness in anesthesia and brain-lesioned patients.

A big-world network in ASD: Dynamical connectivity analysis reflects a deficit in long-range connections and an excess of short-range connections

Over the last years, increasing evidence has fuelled the hypothesis that Autism Spectrum Disorder (ASD) is a condition of altered brain functional connectivity. The great majority of these empirical studies relies on functional magnetic resonance imaging (fMRI) which has a relatively poor temporal resolution. Only a handful of studies has examined networks emerging from dynamic coherence at the millisecond resolution and there are no investigations of coherence at the lowest frequencies in the power spectrum-which has recently been shown to reflect long-range cortico-cortical connections. Here we used electroencephalography (EEG) to assess dynamic brain connectivity in ASD focusing in the low-frequency (delta) range. We found that connectivity patterns were distinct in ASD and control populations and reflected a double dissociation: ASD subjects lacked long-range connections, with a most prominent deficit in fronto-occipital connections. Conversely, individuals with ASD showed increased short-range connections in lateral-frontal electrodes. This effect between categories showed a consistent parametric dependency: as ASD severity increased, short-range coherence was more pronounced and long-range coherence decreased. Theoretical arguments have been proposed arguing that distinct patterns of connectivity may result in networks with different efficiency in transmission of information. We show that the networks in ASD subjects have less Clustering coefficient, greater Characteristic Path Length than controls - indicating that the topology of the network departs from small-world behaviour - and greater modularity. Together these results show that delta-band coherence reveal qualitative and quantitative aspects associated with ASD pathology.

Top-Down Reorganization of Activity in the Visual Pathway after Learning a Shape Identification Task

Learning in shape identification led to global changes in activation across the entire visual pathway, as revealed with whole-brain fMRI. Following extensive training in a shape identification task, brain activity associated with trained shapes relative to the untrained shapes showed: (1) an increased level of activity in retinotopic cortex (RC), (2) a decrease in activation of the lateral occipital cortex (LO), and (3) a decrease in the dorsal attentional network. In addition, RC activations became more correlated (and LO activation, less correlated) with performance. When comparing target-present and target-absent trials within the trained condition, we observed a similar decrease in the dorsal attentional network but not in the visual cortices. These findings indicate a large-scale reorganization of activity in the visual pathway as a result of learning, with the RC becoming more involved (and the LO, less involved) and that these changes are triggered in a top-down manner depending on the perceptual task performed.

A small world of weak ties provides optimal global integration of self-similar modules in functional brain networks

The human brain is organized in functional modules. Such an organization presents a basic conundrum: Modules ought to be sufficiently independent to guarantee functional specialization and sufficiently connected to bind multiple processors for efficient information transfer. It is commonly accepted that small-world architecture of short paths and large local clustering may solve this problem. However, there is intrinsic tension between shortcuts generating small worlds and the persistence of modularity, a global property unrelated to local clustering. Here, we present a possible solution to this puzzle. We first show that a modified percolation theory can define a set of hierarchically organized modules made of strong links in functional brain networks. These modules are “large-world” self-similar structures and, therefore, are far from being small-world. However, incorporating weaker ties to the network converts it into a small world preserving an underlying backbone of well-defined modules. Remarkably, weak ties are precisely organized as predicted by theory maximizing information transfer with minimal wiring cost. This trade-off architecture is reminiscent of the “strength of weak ties” crucial concept of social networks. Such a design suggests a natural solution to the paradox of efficient information flow in the highly modular structure of the brain.

Brain Mechanisms of Serial and Parallel Processing during Dual-Task Performance

The psychological refractory period (PRP) refers to the fact that humans typically cannot perform two tasks at once. Behavioral experiments have led to the proposal that, in fact, peripheral perceptual and motor stages continue to operate in parallel, and that only a central decision stage imposes a serial bottleneck. We tested this model using neuroimaging methods combined with innovative time-sensitive analysis tools. Subjects performed a dual-task visual–auditory paradigm in which a delay of 300 ms was injected into the auditory task either within or outside of the dual-task interference period. Event-related potentials indicated that the first ∼250 ms of processing were insensitive to dual-task interference, and that the PRP was mainly reflected in a delayed global component. By a clustering analysis based on time-resolved functional magnetic resonance imaging, we identified networks with qualitatively different timing properties: sensory areas tracked the objective time of stimulus presentation, a bilateral parietoprefrontal network correlated with the PRP delay, and an extended bilateral network that included bilateral posterior parietal cortex, premotor cortex, supplementary motor area, anterior part of the insula, and cerebellum was shared by both tasks during the extent of dual-task performance. The results provide physiological evidence for the coexistence of serial and parallel processes within a cognitive task.