Generative models, brain function and neuroimaging

The representational capacity and inherent function of any neuron, neuronal population or cortical area in the brain is dynamic and context-sensitive. Functional integration, or interactions among brain systems, that employ driving (bottom up) and backward (top-down) connections, mediate this adaptive and contextual specialisation. A critical consequence is that neuronal responses, in any given cortical area, can represent different things at different times. This can have fundamental implications for the design of brain imaging experiments and the interpretation of their results. Our arguments are developed under generative models of brain function, where higher-level systems provide a prediction of the inputs to lower-level regions. Conflict between the two is resolved by changes in the higher-level representations, which are driven by the ensuing error in lower regions, until the mismatch is "cancelled". From this perspective the specialisation of any region is determined both by bottom-up driving inputs and by top-down predictions. Specialisation is therefore not an intrinsic property of any region but depends on both forward and backward connections with other areas. Because the latter have access to the context in which the inputs are generated they are in a position to modulate the selectivity or specialisation of lower areas. The implications for classical models (e.g., classical receptive fields in electrophysiology, classical specialisation in neuroimaging and connectionism in cognitive models) are severe and suggest these models may provide incomplete accounts of real brain architectures. Here we focus on the implications for cognitive neuroscience in the context of neuroimaging.     

Late maturation of visual hyperacuity

We used a visual evoked–potential measure to study the development of two components of pattern vision, vernier acuity and grating acuity, in humans from early infancy through adolescence. These two visual functions develop at similar rates and have nearly the same absolute values between 1 month and 6 years of age. After age 6, grating acuity is constant at the adult level, but vernier acuity continues to improve, becoming a hyperacuity. Vernier acuity reaches asymptotic levels around age 14 years. These results suggest that adultlike vernier hyperacuity is not limited by spatial resolution or sensitivity of small receptive fields, but rather that the limitation is imposed by higher–level processing. Sensitivity, connections in visual cortical areas, or both therefore retain plasticity throughout childhood and into adolescence.     

Processing spatial relations with different apertures of attention

Neuropsychological studies suggest the existence of lateralized networks that represent categorical and coordinate types of spatial information. In addition, studies with neural networks have shown that they encode more effectively categorical spatial judgments or coordinate spatial judgments, if their input is based, respectively, on units with relatively small, nonoverlapping receptive fields, as opposed to units with relatively large, overlapping receptive fields. These findings leave open the question of whether interactive processes between spatial detectors and types of spatial relations can be modulated by spatial attention. We hypothesized that spreading the attention window to encompass an area that includes two objects promotes coordinate spatial relations, based on coarse coding by large, overlapping, receptive fields. In contrast, narrowing attention to encompass an area that includes only one of the objects benefits categorical spatial relations, by effectively parsing space. By use of a cueing procedure, the spatial attention window was manipulated to select regions of differing areas. As predicted, when the attention window was large, coordinate spatial transformations were noticed faster than categorical transformations; in contrast, when the attention window was relatively smaller, categorical spatial transformations were noticed faster than coordinate transformations. Another novel finding was that coordinate changes were noticed faster when cueing an area that included both objects as well as the empty space between them than when simultaneously cueing both areas including the objects while leaving the gap between them uncued.     

BOLD activation varies parametrically with corner angle throughout human retinotopic cortex

The Alternating Brightness Star (ABS) is an illusion that provides insight into the relationship between brightness perception and corner angle. Recent psychophysical studies of this illusion have shown that corner salience varies parametrically with corner angle, with sharp angles leading to strong illusory percepts and shallow angles leading to weak percepts. It is hypothesized that the illusory effects arise because of an interaction between surface corners and the shape of visual receptive fields: sharp surface corners may create hotspots of high local contrast due to processing by center-surround and other early receptive fields. If this hypothesis is correct, early visual neurons should respond powerfully to sharp corners and curved portions of surface edges. Indeed, the primary role of early visual neurons may be to localize the discontinuities along the edges of surfaces. If so, all early visual areas should show greater BOLD responses to sharp corners than to shallow corners. On the other hand, if corner processing is exclusively constrained to certain areas of the brain, only those specific areas will show greater responses to sharp vs shallow corners. To address this we explored the BOLD correlates of the ABS illusion in the human visual cortex using fMRI. We found that BOLD signal varies parametrically with corner angle throughout the visual cortex, offering the first neurophysiological correlates of the ABS illusion. This finding provides a neurophysiological basis for the previously reported psychophysical data that showed that corner salience varied parametrically with corner angle. We propose that all early visual areas localize discontinuities along the edges of surfaces, and that specific cortical corner-processing circuits further establish the specific nature of those discontinuities, such as their orientation.     

Acetylcholine and olfactory perceptual learning

Olfactory perceptual learning is a relatively long-term, learned increase in perceptual acuity, and has been described in both humans and animals. Data from recent electrophysiological studies have indicated that olfactory perceptual learning may be correlated with changes in odorant receptive fields of neurons in the olfactory bulb and piriform cortex. These changes include enhanced representation of the molecular features of familiar odors by mitral cells in the olfactory bulb, and synthetic coding of multiple coincident odorant features into odor objects by cortical neurons. In this paper, data are reviewed that show the critical role of acetylcholine (Ach) in olfactory system function and plasticity, and cholinergic modulation of olfactory perceptual learning at both the behavioral and cortical level.     

Scopolamine enhances generalization between odor representations in rat olfactory cortex

Acetylcholine (ACh) has a critical, modulatory role in plasticity in many sensory systems. In the rat olfactory system, both behavioral and physiological data indicate that ACh may be required for normal odor memory and synaptic plasticity. Based on these data, neural network models have hypothesized that ACh muscarinic receptors reduce interference between learned cortical representations of odors within the piriform cortex. In this study, odor receptive fields of rat anterior piriform cortex (aPCX) single-units for alkane odors were mapped before and after either a systemic injection of the muscarinic receptor antagonist scopolamine (0.5 mg/kg) or aPCX surface application of 500 μM scopolamine (or saline/ACSF controls). Cross-habituation between alkanes differing by two to four carbons was then examined following a 50-sec habituating stimulus. The results demonstrate that neither aPCX spontaneous activity nor odor-evoked activity (receptive field) was affected by scopolamine, but that cross-habituation in aPCX neurons was enhanced significantly by either systemic or cortical scopolamine. These results indicate that scopolamine selectively enhances generalization between odor representations in aPCX in a simple memory task. Given that ACh primarily affects intracortical association fibers in the aPCX, the results support a role for the association system in odor memory and discrimination and indicate an important ACh modulatory control over this basic sensory process.     

Context-sensitive binding by the laminar circuits of V1 and V2: A unified model of perceptual grouping,attention, and orientation contrast

A detailed neural model is presented of how the laminar circuits of visual cortical areas V1 and V2 implement context-sensitive binding processes such as perceptual grouping and attention. The model proposes how specific laminar circuits allow the responses of visual cortical neurons to be determined not only by the stimuli within their classical receptive fields, but also to be strongly influenced by stimuli in the extra-classical surround. This context-sensitive visual processing can greatly enhance the analysis of visual scenes, especially those containing targets that are low contrast, partially occluded, or crowded by distractors. We show how interactions of feedforward, feedback, and horizontal circuitry can implement several types of contextual processing simultaneously, using shared laminar circuits. In particular, we present computer simulations that suggest how top-down attention and preattentive perceptual grouping, two processes that are fundamental for visual binding, can interact, with attentional enhancement selectively propagating along groupings of both real and illusory contours, thereby showing how attention can selectively enhance object representations. These simulations also illustrate how attention may have a stronger facilitatory effect on low contrast than on high contrast stimuli, and how pop-out from orientation contrast may occur. The specific functional roles which the model proposes for the cortical layers allow several testable neurophysiological predictions to be made. The results presented here simulate only the boundary grouping system of adult cortical architecture. However, we also discuss how this model contributes to a larger neural theory of vision that suggests how intracortical and intercortical feedback help to stabilize development and learning within these cortical circuits. Although feedback plays a key role, fast feedforward processing is possible in response to unambiguous information. Model circuits are capable of synchronizing quickly, but context-sensitive persistence of previous events can influence how synchrony develops. Although these results focus on how the interblob cortical processing stream controls boundary grouping and attention, related modelling of the blob cortical processing stream suggests how visible surfaces are formed, and modelling of the motion stream suggests how transient responses to scenic changes can control long-range apparent motion and also attract spatial attention.     

Picturing peripheral acuity

The grain of the retina becomes progressively coarser from the fovea to the periphery. This is caused by the decreasing number of retinal receptive fields and decreasing amount of cortex devoted to each degree of visual field (= cortical magnification factor) as one goes into the periphery. We simulate this with a picture that is progressively blurred towards its edges; when strictly fixated at its centre looks equally sharp all over.     

Nicotinic modulation of tone-evoked responses in auditory cortex reflects the strength of prior auditory learning

Nicotinic acetylcholine receptors (nAChRs) contribute to sensory-cognitive function, as demonstrated by evidence that nAChR activation enhances, and nAChR blockade impairs, neural processing of sensory stimuli and sensory-cognitive behavior. To better understand the relationship between nAChR function and behavior, here we compare the strength of nAChR-mediated physiology in individual animals to their prior auditory behavioral performance. Adult rats were trained on an auditory-cued, active avoidance task over 4 days and classified as “good,” “intermediate” or “poor” performers based on their initial rate of learning and eventual level of performance. Animals were then anesthetized, and tone-evoked local field potentials (LFPs) recorded in layer 4 of auditory cortex (ACx) before and after a test dose of nicotine (0.7 mg/kg, s.c.) or saline. In “good” performers, nicotine enhanced LFP amplitude and decreased response threshold to characteristic frequency (CF) stimuli, yet had opposite effects (decreased amplitude, increased threshold) on responses to spectrally distant stimuli; i.e., cortical receptive fields became more selective for CF stimuli. In contrast, nicotine had little effect on LFP amplitude in “intermediate” or “poor” performing animals. Nicotine did, however, reduce LFP onset latency in all three groups, indicating that all received an effective dose of the drug. Our findings suggest that nicotinic regulation of cortical receptive fields may be a distinguishing feature of the best-performing animals, and may facilitate sensory-related learning by enhancing receptive field selectivity.     

RELIGIOUS AND MYSTICAL STATES: A NEUROPSYCHOLOGICAL MODEL

Abstract. This paper first considers the current confusion in categorizing and even describing mystical states, including experiences of God, the Void, and lesser religious experiences. The paper presents the necessity of studying the neuropsychological substrate of such experiences both to understand them in greater depth and to help resolve scholarly confusion in this area. As a prelude to presenting a neuropsychological model, the basic principles of brain organization are reviewed, including hemispheri-city; primary, secondary, and tertiary sensory receptive areas; their motor analogues; prefrontosensorial polarity; and the integration of limbic functioning into cortical activity. A neuropsychological model for mystical states is then presented in terms of differential stimulation and deafferentation of various tertiary sensory association areas, along with integration of various patterns of limbic stimulation.     

Cooperative representation of visual borders.

Recently it has been reported that the visual cortical cells which are engaged in cooperative coding of global stimulus features, display synchrony in their firing rates when both are stimulated. Alternative models identify global stimulus features with the course spatial scales of the image. Versions of the Munsterberg or Café Wall illusions which differ in their low spatial frequency content were used to show that in all cases it was the high spatial frequencies in the image which determined the strength and direction of these illusions. Since cells responsive to high spatial frequencies have small receptive fields, cooperative coding must be involved in the representation of long borders in the image.     

Encoding Shape and Spatial Relations: The Role of Receptive Field Size in Coordinating Complementary Representations

An effective functional architecture facilitates interactions among subsystems that are often used together. Computer simulations showed that differences in receptive field sizes can promote such organization. When input was filtered through relatively small nonoverlapping receptive fields, artificial neural net-works learned to categorize shapes relatively quickly; in contrast, when input was filtered through relatively large overlapping receptive fields, networks learned to encode specific shape exemplars or metric spatial relations relatively quickly. Moreover, when the receptive field sizes were allowed to adapt during learning, networks developed smaller receptive fields when they were trained to categorize shapes or spatial relations, and developed larger receptive fields when they were trained to encode specific exemplars or metric distances. In addition, when pairs of networks were constrained to use input from the same type of receptive fields, networks learned a task faster when they were paired with networks that were trained to perform a compatible type of task. Finally, using a novel modular architecture, networks were not preassigned a task, but rather competed to perform the different tasks. Networks with small nonover-lapping receptive fields tended to win the competition for categorical tasks whereas networks with large overlapping receptive fields tended to win the competition for exemplar/metric tasks.     

Is coherent motion an appropriate test for magnocellular sensitivity?

The suggestion that coherent motion may serve as a test of magnocellular sensitivity is problematic. However, the nature of the problems depends on how the "magnocellular system" is defined. If this term is limited to subcortical entities, the problems are that subcortical neurons are not directionally selective, and that their receptive fields are too small to account for the spatial summation of coherent motion. If "magnocellular system" is defined to include cortical entities, such as area MT, one is faced with the fact that this definition itself is problematic as well as the problem that area MT is known to receive parvocellular and koniocellular inputs.     

Representation of visuotactile space in the split brain

Recent neurophysiological research in the monkey has revealed bimodal neuronal cells with both tactile receptive fields on the hand and visual receptive fields that follow the hands as they move, suggesting the existence of a bimodal map of visuotactile space. Using a cross-modal congruency task, we examined the representation of visuotactile space in normal people and in a split-brain patient (J.W.) as the right arm assumed different postures. The results showed that the congruency effects from distracting lights followed the hand around in space in normal people, but failed to do so in the split-brain patient when the hand crossed the midline. This suggests that cross-cortical connections are required to remap visual space to the current hand position when the hand crosses the midline.     

A neural theory of visual attention: bridging cognition and neurophysiology

A neural theory of visual attention (NTVA) is presented. NTVA is a neural interpretation of C. Bundesen's (1990) theory of visual attention (TVA). In NTVA, visual processing capacity is distributed across stimuli by dynamic remapping of receptive fields of cortical cells such that more processing resources (cells) are devoted to behaviorally important objects than to less important ones. By use of the same basic equations used in TVA, NTVA accounts for a wide range of known attentional effects in human performance (reaction times and error rates) and a wide range of effects observed in firing rates of single cells in the primate visual system. NTVA provides a mathematical framework to unify the 2 fields of research--formulas bridging cognition and neurophysiology.     

Neural Mechanisms of Visual Feature Binding Investigated with Microelectrodes and Models

A single object generally activates neurones in many visual cortical areas corresponding to a distributed representation of its features. Itis still under debate how the distributed representation of an objectis bound intoa coherent whole and how unrelated features are separated. Synchronization of neural signals has been proposed to code spatial feature binding, supported by the discovery of synchronized assemblies in visual cortex. Synchronizations are either fast oscillatory (30–90 Hz) cortically generated events, or non-rhythmical stimulus-locked responses, depending on the visual stimulation. The cortical range over which synchronizations occur, transformed to visual space, is generally several times larger than the classical receptive fields (CRF) of neurones in lower visual cortex areas. However, the cortical regions synchronized by fastoscillations do notspan the representational range of larger objects but only parts of it. To relate such restricted segments to perceptual processes the concept of the association field (AF) of local neural assemblies was introduced in accordance with CRFs of single neurones. Here an AF is composed of the aggregate of CRFs of an assembly engaged in a common synchronized state. Itis argued thatspatial continuity of an object is coded by a continuum of overlapping AFs, that is, by overlapping regions of phase coupled neurones. Hence, object continuity would be represented by phase continuity. Besides feature binding, feature separation is necessary for scene segmentation. Separation may be coded by functional decoupling causing uncorrelated activities or by mutual inhibition leading to alternating activations in assemblies of separate representations. A third temporal coding aspect is temporal segmentation by the shortactivation-inhibition cycles of fast oscillations orshorttransientstimulus-locked responses, which may preventperceptual “smearing” by interrupting the flow of visual information into precisely defined frames. The presentpaperalso aims atrelating signals of stimulus dependentsynchronization and desynchronization with basic neural mechanisms and circuits. Finally, the synchronization hypothesis is critically discussed with respect to contradictory psychophysical work and supportive new recording results, including evidence for perception-related synchronizations.     

The critical distance of interaction in the Zöllner illusion

Two experiments attempted to de termine the distance (as visual angle) over which the Zöllner distortion of a straight line could be produced by a background field. Experiment 1 showed that the background lines did not need to intersect the test line in order to distort it but could exert this effect up to a distance of 1 deg visual angle from it. Experiment 2 indicated that when the background lines do intersect the test line portions of these formed beyond an angle of 1 deg do not contribute to the distortion. These values may indicate the size of the cortical receptive fields interacting to produce the illusion.     

Spatially mediated capacity limits in attentive visual perception

Modern theories conceptualize visual selective attention as a competition between objects for the control of cortical receptive fields (RFs). Implicit in this framework is the suggestion that spatially proximal objects, which draw from overlapping pools of RFs, should be more difficult to represent in parallel and with excess capacity than spatially separated objects. The present experiments tested this prediction using analysis of response time distributions in a redundant-targets letter identification task. Data revealed that excess-capacity parallel processing is possible when redundant targets are widely separated within the visual field, but that capacity is near fixed when targets are adjacent. Even at the largest separations tested, however, processing capacity remained strongly limited.     

Reverse correlation in neurophysiology

This article presents a review of reverse correlation in neurophysiology. We discuss the basis of reverse correlation in linear transducers and in spiking neurons. The application of reverse correlation to measure the receptive fields of visual neurons using white noise and m-sequences, and classical findings about spatial and color processing in the cortex resulting from such measurements, are emphasized. Finally, we describe new developments in reverse correlation, including “sub-space” and categorical reverse-correlation. Recent results obtained by applying such methods in the orientation, spatial-frequency and Fourier domains have revealed the importance of cortical inhibition in the establishment of sharp tuning selectivity in single neurons.     

Visual receptive fields and clustering

A pattern recognition technique—clustering—has been used to analyze and evaluate meaningful characteristics of visual receptive fields in the frog tectum. The fields were mapped either by an automatic scanning technique or by a response-feedback method called ALOPEX. The data were then analyzed by the clustering technique, which separates the receptive field into isoresponse regions. The latter can be checked on line by stimulating the eye with each cluster and with combinations of clusters. In this way, existing nonlinearities can be checked objectively.