The role of the posterior parietal cortex in coordinate transformations for visual-motor integration

Lesion to the posterior parietal cortex in monkeys and humans produces spatial deficits in movement and perception. In recording experiments from area 7a, a cortical subdivision in the posterior parietal cortex in monkeys, we have found neurons whose responses are a function of both the retinal location of visual stimuli and the position of the eyes in the orbits. By combining these signals area 7 a neurons code the location of visual stimuli with respect to the head. However, these cells respond over only limited ranges of eye positions (eye-position-dependent coding). To code location in craniotopic space at all eye positions (eye-position-independent coding) an additional step in neural processing is required that uses information distributed across populations of area 7a neurons. We describe here a neural network model, based on back-propagation learning, that both demonstrates how spatial location could be derived from the population response of area 7a neurons and accurately accounts for the observed response properties of these neurons.     

End-to-end neural system identification with neural information flow

Neural information flow (NIF) provides a novel approach for system identification in neuroscience. It models the neural computations in multiple brain regions and can be trained end-to-end via stochastic gradient descent from noninvasive data. NIF models represent neural information processing via a network of coupled tensors, each encoding the representation of the sensory input contained in a brain region. The elements of these tensors can be interpreted as cortical columns whose activity encodes the presence of a specific feature in a spatiotemporal location. Each tensor is coupled to the measured data specific to a brain region via low-rank observation models that can be decomposed into the spatial, temporal and feature receptive fields of a localized neuronal population. Both these observation models and the convolutional weights defining the information processing within regions are learned end-to-end by predicting the neural signal during sensory stimulation. We trained a NIF model on the activity of early visual areas using a large-scale fMRI dataset recorded in a single participant. We show that we can recover plausible visual representations and population receptive fields that are consistent with empirical findings.     

Population-Vector Analysis by Primate Prefrontal Neuron Activities

The population-vector analysis was applied to visualize neuronal processes of sensory-to-motor transformation in the prefrontal cortex while two monkeys performed two types of oculomotor delayed-response (ODR) tasks. In a standard ODR task, monkeys were required to make a quick eye movement to where thevisual cue had been presented 3 s before, whereas in R-ODR task, monkeys wererequired to make an eye movement 90^°clockwise to the direction that the visual cue had been presented. In both tasks, directions of population vectors calculated from cue- and response-period activity were almost the same as cue directions and saccade directions, respectively, indicating that population vectors of cue- and response-period activity represent information of visual inputs and motor outputs, respectively. To visualize neuronal processes of information transformation, population vectors were calculated every 250 ms during a whole trial. In ODR task, population vectors weredirected the same direction as the cue direction during the delay period. However, in R-ODR task, population vector rotated gradually from the direction similar to the cue direction to the saccade direction during the delay period. These results indicate that visual-to-motor transformation occurs during the delay period and that this process can be visualized by the population-vectoranalysis.     

Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity

 A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learning is applied to map place cell activity into action cell activity. The ensemble action cell activity provides navigational maps to support spatial behavior. We present experimental results obtained with a mobile Khepera robot. Received: 02 July 1999 / Accepted in revised form: 20 March 2000     

Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field

The frontal eye field (FEF) participates in selecting the location of behaviorally relevant stimuli for guiding attention and eye movements. We simultaneously recorded local field potentials (LFPs) and spiking activity in the FEF of monkeys performing memory-guided saccade and covert visual search tasks. We compared visual latencies and the time course of spatially selective responses in LFPs and spiking activity. Consistent with the view that LFPs represent synaptic input, visual responses appeared first in the LFPs followed by visual responses in the spiking activity. However, spatially selective activity identifying the location of the target in the visual search array appeared in the spikes about 30 ms before it appeared in the LFPs. Because LFPs reflect dendritic input and spikes measure neuronal output in a local brain region, this temporal relationship suggests that spatial selection necessary for attention and eye movements is computed locally in FEF from spatially nonselective inputs.     

Top-down modulations from dorsal stream in lexical recognition: an effective connectivity FMRI study

Both the ventral and dorsal visual streams in the human brain are known to be involved in reading. However, the interaction of these two pathways and their responses to different cognitive demands remains unclear. In this study, activation of neural pathways during Chinese character reading was acquired by using a functional magnetic resonance imaging (fMRI) technique. Visual-spatial analysis (mediated by the dorsal pathway) was disassociated from lexical recognition (mediated by the ventral pathway) via a spatial-based lexical decision task and effective connectivity analysis. Connectivity results revealed that, during spatial processing, the left superior parietal lobule (SPL) positively modulated the left fusiform gyrus (FG), while during lexical processing, the left SPL received positive modulatory input from the left inferior frontal gyrus (IFG) and sent negative modulatory output to the left FG. These findings suggest that the dorsal stream is highly involved in lexical recognition and acts as a top-down modulator for lexical processing.     

Modality-specific control of strategic spatial attention in parietal cortex

The neural basis of selective spatial attention presents a significant challenge to cognitive neuroscience. Recent neuroimaging studies have suggested that regions of the parietal and temporal cortex constitute a "supramodal" network that mediates goal-directed attention in multiple sensory modalities. Here we used transcranial magnetic stimulation (TMS) to determine which cortical subregions control strategic attention in vision and touch. Healthy observers undertook an orienting task in which a central arrow cue predicted the location of a subsequent visual or somatosensory target. To determine the attentional role of cortical subregions at different stages of processing, TMS was delivered to the right hemisphere during cue or target events. Results indicated a critical role of the inferior parietal cortex in strategic orienting to visual events, but not to somatosensory events. These findings are inconsistent with the existence of a supramodal attentional network and instead provide direct evidence for modality-specific attentional processing in parietal cortex.     

Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey

BACKGROUND: The perceptual ability of humans and monkeys to identify objects in the presence of noise varies systematically and monotonically as a function of how much noise is introduced to the visual display. That is, it becomes more and more difficult to identify an object with increasing noise. Here we examine whether the blood oxygen level-dependent functional magnetic resonance imaging (BOLD fMRI) signal in anesthetized monkeys also shows such monotonic tuning. We employed parametric stimulus sets containing natural images and noise patterns matched for spatial frequency and intensity as well as intermediate images generated by interpolation between natural images and noise patterns. Anesthetized monkeys provide us with the unique opportunity to examine visual processing largely in the absence of top-down cognitive modulations and can thus provide an important baseline against which work with awake monkeys and humans can be compared. RESULTS: We measured BOLD activity in occipital visual cortical areas as natural images and noise patterns, as well as intermediate interpolated patterns at three interpolation levels (25%, 50%, and 75%) were presented to anesthetized monkeys in a block paradigm. We observed reliable visual activity in occipital visual areas including V1, V2, V3, V3A, and V4 as well as the fundus and anterior bank of the superior temporal sulcus (STS). Natural images consistently elicited higher BOLD levels than noise patterns. For intermediate images, however, we did not observe monotonic tuning. Instead, we observed a characteristic V-shaped noise-tuning function in primary and extrastriate visual areas. BOLD signals initially decreased as noise was added to the stimulus but then increased again as the pure noise pattern was approached. We present a simple model based on the number of activated neurons and the strength of activation per neuron that can account for these results. CONCLUSIONS: We show that, for our parametric stimulus set, BOLD activity varied nonmonotonically as a function of how much noise was added to the visual stimuli, unlike the perceptual ability of humans and monkeys to identify such stimuli. This raises important caveats for interpreting fMRI data and demonstrates the importance of assessing not only which neural populations are activated by contrasting conditions during an fMRI study, but also the strength of this activation. This becomes particularly important when using the BOLD signal to make inferences about the relationship between neural activity and behavior.     

Single neurons in posterior parietal cortex of monkeys encode cognitive set

The primate posterior parietal cortex (PPC), part of the dorsal visual pathway, is best known for its role in encoding salient spatial information. Yet there are indications that neural activity in the PPC can also be modulated by nonspatial task-related information. In this study, we tested whether neurons in the PPC encode signals related to cognitive set, that is, the preparation to perform a particular task. Cognitive set has previously been associated with the frontal cortex but not the PPC. In this study, monkeys performed a cognitive set shifting paradigm in which they were cued in advance to apply one of two different task rules to the subsequent stimulus on every trial. Here we show that a subset of neurons in the PPC, concentrated in the lateral bank of the intraparietal sulcus and on the angular gyrus, responds selectively to cues for different task rules.     

Multimodal integration for the representation of space in the posterior parietal cortex.

The posterior parietal cortex has long been considered an ''association'' area that combines information from different sensory modalities to form a cognitive representation of space. However, until recently little has been known about the neural mechanisms responsible for this important cognitive process. Recent experiments from the author''s laboratory indicate that visual, somatosensory, auditory and vestibular signals are combined in areas LIP and 7a of the posterior parietal cortex. The integration of these signals can represent the locations of stimuli with respect to the observer and within the environment. Area MSTd combines visual motion signals, similar to those generated during an observer''s movement through the environment, with eye-movement and vestibular signals. This integration appears to play a role in specifying the path on which the observer is moving. All three cortical areas combine different modalities into common spatial frames by using a gain-field mechanism. The spatial representations in areas LIP and 7a appear to be important for specifying the locations of targets for actions such as eye movements or reaching; the spatial representation within area MSTd appears to be important for navigation and the perceptual stability of motion signals.     

Fix your eyes in the space you could reach: neurons in the macaque medial parietal cortex prefer gaze positions in peripersonal space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping.     

Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory

We compared behavioral and neural effects of cholinergic enhancement between spatial attention, spatial working memory (WM), and visual control tasks, using fMRI and the anticholinesterase physostigmine. Physostigmine speeded responses nonselectively but increased accuracy selectively for attention. Physostigmine also decreased activations to visual stimulation across all tasks within primary visual cortex, increased extrastriate occipital cortex activation selectively during maintained attention and WM encoding, and decreased parietal activation selectively during maintained attention. Finally, lateralization of occipital activation as a function of the visual hemifield toward which attention or memory was directed was decreased under physostigmine. In the case of attention, this effect correlated strongly with a decrease in a behavioral measure of selective spatial processing. Our results suggest that, while cholinergic enhancement facilitates visual attention by increasing activity in extrastriate cortex generally, it accomplishes this in a manner that reduces expectation-driven selective biasing of extrastriate cortex.     

Tracking the mind's image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery

The functional relevance of brain activity during visuospatial tasks was investigated by combining functional magnetic resonance imaging with unilateral repetitive transcranial magnetic stimulation (rTMS). The cognitive tasks involved visuospatial operations on visually presented and mentally imagined material ("mental clock task"). While visuospatial operations were associated with activation of the intraparietal sulcus region bilaterally, only the group which received rTMS to the right parietal lobe showed an impairment of performance during and immediately after rTMS. This functional parietal asymmetry might indicate a capacity of the right parietal lobe to compensate for a temporary suppression of the left. This is compatible with current theories of spatial hemineglect and constitutes a constraint for models of distributed information processing in the parietal lobes.     

Seeing more than meets the eye: processing of illusory contours in animals

This review article illustrates that mammals, birds and insects are able to perceive illusory contours. Illusory contours lack a physical counterpart, but monkeys, cats, owls and bees perceive them as if they were real borders. In all of these species, a neural correlate for such perceptual completion phenomena has been described. The robustness of neuronal responses and the abundance of cells argue that such neurons might indeed represent a neural correlate for illusory contour perception. The internal state of an animal subject (i.e., alert and behaving) seems to be an important factor when correlating neural activity with perceptual phenomena. The fact that the neural network necessary for illusory contour perception has been found in relatively early visual brain areas in all tested animals suggests that bottom-up processing is largely sufficient to explain such perceptual abilities. However, recent findings in monkeys indicate that feedback loops within the visual system may provide additional modulation. The detection of illusory contours by independently evolved visual systems argues that processing of edges in the absence of contrast gradients reflects fundamental visual constraints and not just an artifact of visual processing.     

Spike suppression in a local cortical circuit induced by transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) noninvasively interferes with human cortical function, and is widely used as an effective technique for probing causal links between neural activity and cognitive function. However, the physiological mechanisms underlying TMS-induced effects on neural activity remain unclear. We examined the mechanism by which TMS disrupts neural activity in a local circuit in early visual cortex using a computational model consisting of conductance-based spiking neurons with excitatory and inhibitory synaptic connections. We found that single-pulse TMS suppressed spiking activity in a local circuit model, disrupting the population response. Spike suppression was observed when TMS was applied to the local circuit within a limited time window after the local circuit received sensory afferent input, as observed in experiments investigating suppression of visual perception with TMS targeting early visual cortex. Quantitative analyses revealed that the magnitude of suppression was significantly larger for synaptically-connected neurons than for isolated individual neurons, suggesting that intracortical inhibitory synaptic coupling also plays an important role in TMS-induced suppression. A conventional local circuit model of early visual cortex explained only the early period of visual suppression observed in experiments. However, models either involving strong recurrent excitatory synaptic connections or sustained excitatory input were able to reproduce the late period of visual suppression. These results suggest that TMS targeting early visual cortex disrupts functionally distinct neural signals, possibly corresponding to feedforward and recurrent information processing, by imposing inhibitory effects through intracortical inhibitory synaptic connections.     

Encoding of Naturalistic Stimuli by Local Field Potential Spectra in Networks of Excitatory and Inhibitory Neurons

Recordings of local field potentials (LFPs) reveal that the sensory cortex displays rhythmic activity and fluctuations over a wide range of frequencies and amplitudes. Yet, the role of this kind of activity in encoding sensory information remains largely unknown. To understand the rules of translation between the structure of sensory stimuli and the fluctuations of cortical responses, we simulated a sparsely connected network of excitatory and inhibitory neurons modeling a local cortical population, and we determined how the LFPs generated by the network encode information about input stimuli. We first considered simple static and periodic stimuli and then naturalistic input stimuli based on electrophysiological recordings from the thalamus of anesthetized monkeys watching natural movie scenes. We found that the simulated network produced stimulus-related LFP changes that were in striking agreement with the LFPs obtained from the primary visual cortex. Moreover, our results demonstrate that the network encoded static input spike rates into gamma-range oscillations generated by inhibitory–excitatory neural interactions and encoded slow dynamic features of the input into slow LFP fluctuations mediated by stimulus–neural interactions. The model cortical network processed dynamic stimuli with naturalistic temporal structure by using low and high response frequencies as independent communication channels, again in agreement with recent reports from visual cortex responses to naturalistic movies. One potential function of this frequency decomposition into independent information channels operated by the cortical network may be that of enhancing the capacity of the cortical column to encode our complex sensory environment.     

Maps of space in human frontoparietal cortex

Prefrontal cortex (PFC) and posterior parietal cortex (PPC) are neural substrates for spatial cognition. We here review studies in which we tested the hypothesis that human frontoparietal cortex may function as a priority map. According to priority map theory, objects or locations in the visual world are represented by neural activity that is proportional to their attentional priority. Using functional magnetic resonance imaging (fMRI), we first identified topographic maps in PFC and PPC as candidate priority maps of space. We then measured fMRI activity in candidate priority maps during the delay periods of a covert attention task, a spatial working memory task, and a motor planning task to test whether the activity depended on the particular spatial cognition. Our hypothesis was that some, but not all, candidate priority maps in PFC and PPC would be agnostic with regard to what was being prioritized, in that their activity would reflect the location in space across tasks rather than a particular kind of spatial cognition (e.g., covert attention). To test whether patterns of delay period activity were interchangeable during the spatial cognitive tasks, we used multivariate classifiers. We found that decoders trained to predict the locations on one task (e.g., working memory) cross-predicted the locations on the other tasks (e.g., covert attention and motor planning) in superior precentral sulcus (sPCS) and in a region of intraparietal sulcus (IPS2), suggesting that these patterns of maintenance activity may be interchangeable across the tasks. Such properties make sPCS in frontal cortex and IPS2 in parietal cortex viable priority map candidates, and suggest that these areas may be the human homologs of the monkey frontal eye field (FEF) and lateral intraparietal area (LIP).     

The role of attention in figure-ground segregation in areas V1 and V4 of the visual cortex

Our visual system segments images into objects and background. Figure-ground segregation relies on the detection of feature discontinuities that signal boundaries between the figures and the background and on a complementary region-filling process that groups together image regions with similar features. The neuronal mechanisms for these processes are not well understood and it is unknown how they depend on visual attention. We measured neuronal activity in V1 and V4 in a task where monkeys either made an eye movement to texture-defined figures or ignored them. V1 activity predicted the timing and the direction of the saccade if the figures were task relevant. We found that boundary detection is an early process that depends little on attention, whereas region filling occurs later and is facilitated by visual attention, which acts in an object-based manner. Our findings are explained by a model with local, bottom-up computations for boundary detection and feedback processing for region filling.     

Spatial-area selective retrieval of multiple object–place associations in a hierarchical cognitive map formed by theta phase coding

The human cognitive map is known to be hierarchically organized consisting of a set of perceptually clustered landmarks. Patient studies have demonstrated that these cognitive maps are maintained by the hippocampus, while the neural dynamics are still poorly understood. The authors have shown that the neural dynamic “theta phase precession” observed in the rodent hippocampus may be capable of forming hierarchical cognitive maps in humans. In the model, a visual input sequence consisting of object and scene features in the central and peripheral visual fields, respectively, results in the formation of a hierarchical cognitive map for object–place associations. Surprisingly, it is possible for such a complex memory structure to be formed in a few seconds. In this paper, we evaluate the memory retrieval of object–place associations in the hierarchical network formed by theta phase precession. The results show that multiple object–place associations can be retrieved with the initial cue of a scene input. Importantly, according to the wide-to-narrow unidirectional connections among scene units, the spatial area for object–place retrieval can be controlled by the spatial area of the initial cue input. These results indicate that the hierarchical cognitive maps have computational advantages on a spatial-area selective retrieval of multiple object–place associations. Theta phase precession dynamics is suggested as a fundamental neural mechanism of the human cognitive map.     

Neuronal assemblies: single cortical neurons are obedient members of a huge orchestra

Spontaneous cortical activity of single neurons is often either dismissed as noise, or is regarded as carrying no functional significance and hence is ignored. Our findings suggest that such concepts should be revised. We explored the coherent population activity of neuronal assemblies in primary sensory area in the absence of a sensory input. Recent advances in real-time optical imaging based on voltage-sensitive dyes (VSDI) have facilitated exploration of population activity and its intimate relationship to the activity of individual cortical neurons. It has been shown by in vivo intracellular recordings that the dye signal measures the sum of the membrane potential changes in all the neuronal elements in the imaged area, emphasizing subthreshold synaptic potentials and dendritic action potentials in neuronal arborizations originating from neurons in all cortical layers whose dendrites reach the superficial cortical layers. Thus, the VSDI has allowed us to image the rather illusive activity in neuronal dendrites that cannot be readily explored by single unit recordings. Surprisingly, we found that the amplitude of this type of ongoing subthreshold activity is of the same order of magnitude as evoked activity. We also found that this ongoing activity exhibited high synchronization over many millimeters of cortex. We then investigated the influence of ongoing activity on the evoked response, and showed that the two interact strongly. Furthermore, we found that cortical states that were previously associated only with evoked activity can actually be observed also in the absence of stimulation, for example, the cortical representation of a given orientation may appear without any visual input. This demonstration suggests that ongoing activity may also play a major role in other cortical function by providing a neuronal substrate for the dependence of sensory information processing on context, behavior, memory and other aspects of cognitive function.