Dynamic and stable population coding of attentional instructions coexist in the prefrontal cortex.

A large body of recent work suggests that neural representations in prefrontal cortex (PFC) are changing over time to adapt to task demands. However, it remains unclear whether and how such dynamic coding schemes depend on the encoded variable and are influenced by anatomical constraints. Using a cued attention task and multivariate classification methods, we show that neuronal ensembles in PFC encode and retain in working memory spatial and color attentional instructions in an anatomically specific manner. Spatial instructions could be decoded both from the frontal eye field (FEF) and the ventrolateral PFC (vlPFC) population, albeit more robustly from FEF, whereas color instructions were decoded more robustly from vlPFC. Decoding spatial and color information from vlPFC activity in the high-dimensional state space indicated stronger dynamics for color, across the cue presentation and memory periods. The change in the color code was largely due to rapid changes in the network state during the transition to the delay period. However, we found that dynamic vlPFC activity contained time-invariant color information within a low-dimensional subspace of neural activity that allowed for stable decoding of color across time. Furthermore, spatial attention influenced decoding of stimuli features profoundly in vlPFC, but less so in visual area V4. Overall, our results suggest that dynamic population coding of attentional instructions within PFC is shaped by anatomical constraints and can coexist with stable subspace coding that allows time-invariant decoding of information about the future target.

Distinct roles of prefrontal and parietal areas in the encoding of attentional priority.

When searching for an object in a crowded scene, information about the similarity of stimuli to the target object is thought to be encoded in spatial priority maps, which are subsequently used to guide shifts of attention and gaze to likely targets. Two key cortical areas that have been described as holding priority maps are the frontal eye field (FEF) and the lateral intraparietal area (LIP). However, little is known about their distinct contributions in priority encoding. Here, we compared neuronal responses in FEF and LIP during free-viewing visual search. Although saccade selection signals emerged earlier in FEF, information about the target emerged at similar latencies in distinct populations within the two areas. Notably, however, effects in FEF were more pronounced. Moreover, LIP neurons encoded the similarity of stimuli to the target independent of saccade selection, whereas in FEF, encoding of target similarity was strongly modulated by saccade selection. Taken together, our findings suggest hierarchical processing of saccade selection signals and parallel processing of feature-based attention signals within the parietofrontal network with FEF having a more prominent role in priority encoding. Furthermore, they suggest discrete roles of FEF and LIP in the construction of priority maps.

Neural signatures of attention: insights from decoding population activity patterns.

Understanding brain function and the computations that individual neurons and neuronal ensembles carry out during cognitive functions is one of the biggest challenges in neuroscientific research. To this end, invasive electrophysiological studies have provided important insights by recording the activity of single neurons in behaving animals. To average out noise, responses are typically averaged across repetitions and across neurons that are usually recorded on different days. However, the brain makes decisions on short time scales based on limited exposure to sensory stimulation by interpreting responses of populations of neurons on a moment to moment basis. Recent studies have employed machine-learning algorithms in attention and other cognitive tasks to decode the information content of distributed activity patterns across neuronal ensembles on a single trial basis. Here, we review results from studies that have used pattern-classification decoding approaches to explore the population representation of cognitive functions. These studies have offered significant insights into population coding mechanisms. Moreover, we discuss how such advances can aid the development of cognitive brain-computer interfaces.

Top-Down Control of Visual Attention by the Prefrontal Cortex. Functional Specialization and Long-Range Interactions.

The ability to select information that is relevant to current behavioral goals is the hallmark of voluntary attention and an essential part of our cognition. Attention tasks are a prime example to study at the neuronal level, how task related information can be selectively processed in the brain while irrelevant information is filtered out. Whereas, numerous studies have focused on elucidating the mechanisms of visual attention at the single neuron and population level in the visual cortices, considerably less work has been devoted to deciphering the distinct contribution of higher-order brain areas, which are known to be critical for the employment of attention. Among these areas, the prefrontal cortex (PFC) has long been considered a source of top-down signals that bias selection in early visual areas in favor of the attended features. Here, we review recent experimental data that support the role of PFC in attention. We examine the existing evidence for functional specialization within PFC and we discuss how long-range interactions between PFC subregions and posterior visual areas may be implemented in the brain and contribute to the attentional modulation of different measures of neural activity in visual cortices.

Oscillatory synchrony as a mechanism of attentional processing.

The question of how the brain selects which stimuli in our visual field will be given priority to enter into perception, to guide our actions and to form our memories has been a matter of intense research in studies of visual attention. Work in humans and animal models has revealed an extended network of areas involved in the control and maintenance of attention. For many years, imaging studies in humans constituted the main source of a systems level approach, while electrophysiological recordings in non-human primates provided insight into the cellular mechanisms of visual attention. Recent technological advances and the development of sophisticated analytical tools have allowed us to bridge the gap between the two approaches and assess how neuronal ensembles across a distributed network of areas interact in visual attention tasks. A growing body of evidence suggests that oscillatory synchrony plays a crucial role in the selective communication of neuronal populations that encode the attended stimuli. Here, we discuss data from theoretical and electrophysiological studies, with more emphasis on findings from humans and non-human primates that point to the relevance of oscillatory activity and synchrony for attentional processing and behavior. These findings suggest that oscillatory synchrony in specific frequencies reflects the biophysical properties of specific cell types and local circuits and allows the brain to dynamically switch between different spatio-temporal patterns of activity to achieve flexible integration and selective routing of information along selected neuronal populations according to behavioral demands. This article is part of a Special Issue entitled SI: Prediction and Attention.

Topography of Visuomotor Parameters in the Frontal and Premotor Eye Fields.

To determine whether the periarcuate frontal cortex spatially encodes visual and oculomotor parameters, we trained monkeys to repeatedly execute saccades of the same amplitude and direction toward visual targets and we obtained quantitative images of the distribution of metabolic activity in 2D flattened reconstructions of the arcuate sulcus (As) and prearcuate convexity. We found two topographic maps of contraversive saccades to visual targets, separated by a region representing the vertical meridian: the first region straddled the fundus of the As and occupied areas 44 and 6-ventral, whereas the second one occupied areas 8A and 45 in the anterior bank of the As and the prearcuate convexity. The representation of the vertical meridian runs along the posterior borders of areas 8A and 45 (deep in the As). In both maps, the upper part of visuo-oculomotor space is represented ventrally and laterally and the lower part dorsally and medially whereas dorsal and ventral regions are separated by the representation of the horizontal meridian.

Lesions of prefrontal cortex reduce attentional modulation of neuronal responses and synchrony in V4.

It is widely held that the frontal eye field (FEF) in prefrontal cortex (PFC) modulates processing in visual cortex with attention, although the evidence that it is necessary is equivocal. To help identify critical sources of attentional feedback to area V4, we surgically removed the entire lateral PFC, including the FEF, in one hemisphere and transected the corpus callosum and anterior commissure in two macaques. This deprived V4 of PFC input in one hemisphere while keeping the other hemisphere intact. In the absence of PFC, attentional effects on neuronal responses and synchrony in V4 were substantially reduced and the remaining effects of attention were delayed in time, indicating a critical role for PFC. Conversely, distracters captured attention and influenced V4 responses. However, because the effects of attention in V4 were not eliminated by PFC lesions, other sources of top-down attentional control signals to visual cortex must exist outside of PFC.

A procedure for testing across-condition rhythmic spike-field association change.

Many experiments in neuroscience have compared the strength of association between neural spike trains and rhythms present in local field potential (LFP) recordings. The measure employed in these comparisons, "spike-field coherence", is a frequency dependent measure of linear association, and is shown to depend on overall neural activity (Lepage et al., 2011). Dependence upon overall neural activity, that is, dependence upon the total number of spikes, renders comparison of spike-field coherence across experimental context difficult. In this paper, an inferential procedure based upon a generalized linear model is shown to be capable of separating the effects of overall neural activity from spike train-LFP oscillatory coupling. This separation provides a means to compare the strength of oscillatory association between spike train-LFP pairs independent of differences in spike counts. Following a review of the generalized linear modelling framework of point process neural activity a specific class of generalized linear models are introduced. This model class, using either a piece-wise constant link function, or an exponential function to relate an LFP rhythm to neural response, is used to develop hypothesis tests capable of detecting changes in spike train-LFP oscillatory coupling. The performance of these tests is validated, both in simulation and on real data. The proposed method of inference provides a principled statistical procedure by which across-context change in spike train-LFP rhythmic association can be directly inferred that explicitly handles between-condition differences in total spike count.

Cell-type-specific synchronization of neural activity in FEF with V4 during attention.

Shifts of gaze and shifts of attention are closely linked and it is debated whether they result from the same neural mechanisms. Both processes involve the frontal eye fields (FEF), an area which is also a source of top-down feedback to area V4 during covert attention. To test the relative contributions of oculomotor and attention-related FEF signals to such feedback, we recorded simultaneously from both areas in a covert attention task and in a saccade task. In the attention task, only visual and visuomovement FEF neurons showed enhanced responses, whereas movement cells were unchanged. Importantly, visual, but not movement or visuomovement cells, showed enhanced gamma frequency synchronization with activity in V4 during attention. Within FEF, beta synchronization was increased for movement cells during attention but was suppressed in the saccade task. These findings support the idea that the attentional modulation of visual processing is not mediated by movement neurons.

The place code of saccade metrics in the lateral bank of the intraparietal sulcus.

The lateral intraparietal area (LIP) of monkeys is known to participate in the guidance of rapid eye movements (saccades), but the means it uses to specify movement variables are poorly understood. To determine whether area LIP devotes neural space to encode saccade metrics spatially, we used the quantitative [(14)C]deoxyglucose method to obtain images of the distribution of metabolic activity in the intraparietal sulcus (IPs) of rhesus monkeys trained to repeatedly execute saccades of the same amplitude and direction for the duration of the experiment. Different monkeys were trained to perform saccades of different sizes and in different directions. A clear topography of saccade metrics was found in the cytoarchitectonically identified area LIP ventral (LIPv) contralateral to the direction of the eye movements. We demonstrate that the representation of the vertical meridian runs parallel to the fundus of the IPs and that it is not orthogonal to the representation of the horizontal meridian. Instead, the latter runs through the middle of LIPv parallel to its border with area LIP dorsal (LIPd). The upper part of oculomotor space is represented rostrally and dorsally relative to the horizontal meridian toward the LIPv-LIPd border, whereas the lower part of oculomotor space is represented caudally and ventrally toward the caudal edge of the IPs. Saccade amplitude is also represented in an orderly manner.

Long-range neural coupling through synchronization with attention.

In a crowded visual scene, we typically employ attention to select stimuli that are behaviorally relevant. Two likely cortical sources of top-down attentional feedback to cortical visual areas are the prefrontal (PFC) and posterior parietal (PPC) cortices. Recent neurophysiological studies show that areas in PFC and PPC process signals about the locus of attention earlier than in extrastriate visual areas and are therefore likely to mediate attentional selection. Moreover, attentional selection appears to be mediated in part by neural synchrony between neurons in PFC/PPC and early visual areas, with phase relationships that seem optimal for increasing the impact of the top-down inputs to the visual cortex.

High-frequency, long-range coupling between prefrontal and visual cortex during attention.

Electrical recordings in humans and monkeys show attentional enhancement of evoked responses and gamma synchrony in ventral stream cortical areas. Does this synchrony result from intrinsic activity in visual cortex or from inputs from other structures? Using paired recordings in the frontal eye field (FEF) and area V4, we found that attention to a stimulus in their joint receptive field leads to enhanced oscillatory coupling between the two areas, particularly at gamma frequencies. This coupling appeared to be initiated by FEF and was time-shifted by about 8 to 13 milliseconds across a range of frequencies. Considering the expected conduction and synaptic delays between the areas, this time-shifted coupling at gamma frequencies may optimize the postsynaptic impact of spikes from one area upon the other, improving cross-area communication with attention.

Saccade-related information in the superior temporal motion complex: quantitative functional mapping in the monkey.

Although the role of the motion complex [cortical areas middle temporal (V5/MT), medial superior temporal (MST), and fundus of the superior temporal (FST)] in visual motion and smooth-pursuit eye movements is well understood, little is known about its involvement in rapid eye movements (saccades). To address this issue, we used the quantitative 14C-deoxyglucose method to obtain functional maps of the cerebral cortex lying in the superior temporal sulcus of rhesus monkeys executing saccades to visual targets and saccades to memorized targets in complete darkness. Fixational effects were observed in MT-foveal, FST, the anterior part of V4-transitional (V4t), and temporal-occipital areas. Saccades to memorized targets activated areas V5/MT, MST, and V4t, which were also activated for saccades to visual targets. Regions activated in the light and in the dark overlapped extensively. In addition, saccades to visual targets activated areas FST and the intermediate part of the polysensory temporal-parietal-occipital area. Cortical activity related to visually guided saccades could be explained, at least in part, by visual motion. Because only oculomotor signals can account for the equally robust activations induced by memory saccades in complete darkness, we suggest that areas V5/MT, MST, and V4t receive and/or process saccade-related oculomotor information.

Architectonic organization of the inferior parietal convexity of the macaque monkey.

The inferior parietal lobule (IPL) of the macaque monkey constitutes the largest part of Brodmann's area 7. Functional, connectional, and architectonic data have indicated that area 7 is comprised of several distinct sectors located in the lateral bank of the intraparietal sulcus and on the IPL cortical convexity. To date, however, attempts to parcellate the IPL based on architectonic criteria have been controversial, and correlation between anatomical and functional data has been inadequate. In the present study we aimed to determine the number and extent of cytoarchitectonically distinct areas occupying the IPL convexity. To this end, we studied the cytoarchitecture and myeloarchitecture of this region in 28 hemispheres of 17 macaque monkeys. Four distinct areas were identified at different rostrocaudal levels along the IPL convexity and were defined as PF, PFG, PG, and Opt, with area PF corresponding to the rostralmost area and area Opt to the caudalmost one. All areas extend dorsally up to the lateral bank of the intraparietal sulcus, for about 1-2 mm. Areas PF, PFG, and PG border ventrally on opercular areas, whereas area Opt extends ventrally into the dorsal bank of the superior temporal sulcus. Analysis of the distribution of SMI-32 immunoreactivity confirmed the proposed parcellation scheme. Some additional connectional data showed that the four areas project in a differential way to the premotor cortex. The present data challenge the current widely used subdivision of the IPL convexity into two areas, confirming, but also extending the subdivision originally proposed by Pandya and Seltzer.

Cortical connections of the inferior parietal cortical convexity of the macaque monkey.

We traced the cortical connections of the 4 cytoarchitectonic fields--Opt, PG, PFG, PF--forming the cortical convexity of the macaque inferior parietal lobule (IPL). Each of these fields displayed markedly distinct sets of connections. Although Opt and PG are both targets of dorsal visual stream and temporal visual areas, PG is also target of somatosensory and auditory areas. Primary parietal and frontal connections of Opt include area PGm and eye-related areas. In contrast, major parietal and frontal connections of PG include IPL, caudal superior parietal lobule (SPL), and agranular frontal arm-related areas. PFG is target of somatosensory areas and also of the medial superior temporal area (MST) and temporal visual areas and is connected with IPL, rostral SPL, and ventral premotor arm- and face-related areas. Finally, PF is primarily connected with somatosensory areas and with parietal and frontal face- and arm-related areas. The present data challenge the bipartite subdivision of the IPL convexity into a caudal and a rostral area (7a and 7b, respectively) and provide a new anatomical frame of reference of the macaque IPL convexity that advances our present knowledge on the functional organization of this cortical sector, giving new insight into its possible role in space perception and motor control.

When vision guides movement: a functional imaging study of the monkey brain.

Goal-directed reaching requires a precise neural representation of the arm position and the target location. Parietal and frontal cortical areas rely on visual, somatosensory, and motor signals to guide the reaching arm to the desired position in space. To dissociate the regions processing these signals, we applied the quantitative [(14)C]-deoxyglucose method on monkeys reaching either in the light or in the dark. Nonvisual (somatosensory and memory-related) guidance of the arm, during reaching in the dark, induced activation of discrete regions in the parietal, premotor, and motor cortices. These included the dorsal part of the medial bank of the intraparietal sulcus, the ventral premotor area F4, the dorsal premotor area F2 below the superior precentral dimple, and the primary somatosensory and motor cortices. Additional parietal and premotor regions comprising the ventral intraparietal cortex, ventral premotor area F5, and the ventral part of dorsal premotor area F2 were activated by visual guidance of the arm during reaching in the light. This study provides evidence that different regions of the parieto-premotor circuit process the visual, somatosensory, and motor-memory-related signals which guide the moving arm.