Aldo Genovesio

Prefrontal Cortex Activity Related to Abstract Response Strategies

Many monkeys adopt abstract response strategies as they learn to map visual symbols to responses by trial and error. According to the repeat-stay strategy, if a symbol repeats from a previous, successful trial, the monkeys should stay with their most recent response choice. According to the change-shift strategy, if the symbol changes, the monkeys should shift to a different choice. We recorded the activity of prefrontal cortex neurons while monkeys chose responses according to these two strategies. Many neurons had activity selective for the strategy used. In a subsequent block of trials, the monkeys learned fixed stimulus-response mappings with the same stimuli. Some neurons had activity selective for choosing responses based on fixed mappings, others for choosing based on abstract strategies. These findings indicate that the prefrontal cortex contributes to the implementation of the abstract response strategies that monkeys use during trial-and-error learning.

Early coding of reaching: frontal and parietal association connections of parieto-occipital cortex.

The ipsilateral association connections of the cortex of the dorsal part of the rostral bank of the parieto‐occipital sulcus and of the adjoining posterior part of the superior parietal lobule were studied by using different retrograde flourescent tracers. Fluoro‐Ruby, Fast blue and Diamidino yellow were injected into visual area V6A, and dorso‐caudal (PMdc, F2) and dorso‐rostral (PMdr, F7) premotor cortex, respectively. The parietal area of injection had been previously characterized physiologically in behaving monkeys, through a variety of oculomotor and visuomanual tasks. Area V6A is mainly linked by reciprocal projections to parietal areas 7m, MIP (medial intraparietal) and PEa, and, to a lesser extent, to frontal areas PMdr (rostral dorsal premotor cortex, F7) and PMdc (F2). All these areas project to that part of the dorsocaudal premotor cortex that has a direct access to primary motor cortex. V6A is also connected to area F5 and, to a lesser extent, to 7a, ventral (VIP) and lateral (LIP) intraparietal areas. This pattern of association connections may explain the presence of visually‐related and eye‐position signals in premotor cortex, as well as the influence of information concerning arm position and movement direction on V6A neural activity. Area V6A emerges as a potential ‘early’ node of the distributed network underlying visually‐guided reaching. In this network, reciprocal association connections probably impose, through re‐entrant signalling, a recursive property to the operations leading to the composition of eye and hand motor commands.

Callosal connections of dorso-lateral premotor cortex

This study investigated the organization of the callosal connections of the two subdivisions of the monkey dorsal premotor cortex (PMd), dorso‐rostral (F7) and dorso‐caudal (F2). In one animal, Fast blue and Diamidino yellow were injected in F7 and F2, respectively; in a second animal, the pattern of injections was reversed. F7 and F2 receive a major callosal input from their homotopic counterpart. The heterotopic connections of F7 originate mainly from F2, with smaller contingent from pre‐supplementary motor area (pre‐SMA, F6), area 8 (frontal eye fields), and prefrontal cortex (area 46), while those of F2 originate from F7, with smaller contributions from ventral premotor areas (F5, F4), SMA‐proper (F3), and primary motor cortex (M1). Callosal cells projecting homotopically are mostly located in layers II–III, those projecting heterotopically occupy layers II–III and V–VI. A spectral analysis was used to characterize the spatial fluctuations of the distribution of callosal neurons, in both F7 and F2, as well as in adjacent cortical areas. The results revealed two main periodic components. The first, in the domain of the low spatial frequencies, corresponds to periodicities of cell density with peak‐to‐peak distances of approximately 10 mm, and suggests an arrangement of callosal cells in the form of 5‐mm wide bands. The second corresponds to periodicities of approximately 2 mm, and probably reflects a 1‐mm columnar‐like arrangement. Coherency and phase analyses showed that, although similar in their spatial arrangements, callosal cells projecting to dorsal premotor areas are segregated in the tangential cortical domain.

Frontal pole cortex: Encoding ends at the end of the endbrain

Considerable neuroimaging research in humans indicates that the frontal pole cortex (FPC), also known as Brodmann area 10, contributes to many aspects of cognition. Despite these findings, however, its fundamental function and mechanism remain unclear. Recent neurophysiological results from the FPC of monkeys have implications about both. Neurons in the FPC seem to encode chosen goals at feedback time and nothing else. Goals, the places and objects that serve as targets for action, come in many forms and arise from many cognitive processes. The FPCs signal, although surprisingly simple for neurons at the apex of a prefrontal hierarchy, could promote learning about which kinds of goals and goal-generating processes produce particular costs and benefits, thereby improving future choices.

Monkey Orbitofrontal Cortex Encodes Response Choices Near Feedback Time

The primate prefrontal cortex contributes to stimulus-guided behavior, but the functional specializations among its areas remain uncertain. To better understand such specializations, we contrasted neuronal activity in the dorsolateral prefrontal cortex (PFdl) and the orbital prefrontal cortex (PFo). The task required rhesus monkeys to use a visual cue to choose a saccade target. Some cues instructed the monkeys to repeat their most recent response; others instructed them to change it. Responses were followed by feedback: fluid reward if correct, visual feedback if incorrect. Previous studies, using different tasks, have reported that PFo neurons did not encode responses. We found PFo did encode responses in this task, but only near feedback time, after the response had been completed. PFdl differed from PFo in several respects. As reported previously, some PFdl neurons encoded responses from the previous trial and others encoded planned responses. PFo neurons did not have these properties. After feedback, PFdl encoded rewarded responses better than unrewarded ones and thus combined response and outcome information. PFo, in contrast, encoded the responses chosen, rewarded or not. These findings suggest that PFdl and PFo contribute differently to response knowledge, with PFo using an outcome-independent signal to monitor current responses at feedback time.

Prefrontal–parietal function: from foraging to foresight

Comparative neuroanatomy shows that new prefrontal areas emerged during the evolution of anthropoid primates to augment prefrontal, parietal, and temporal areas that had evolved in earlier primates. We recently proposed that the new anthropoid areas reduce foraging errors by generating goals from current contexts and learning to do so rapidly, sometimes based on single events. Among the contexts used to generate these goals, the posterior parietal cortex provides the new prefrontal areas with information about relational metrics such as order, number, duration, length, distance and proportion, which play a crucial role in foraging choices. Here we propose that this specialized network later became adapted to support the human capacity for reasoning and general problem-solving.

Reaching in Depth: Hand Position Dominates over Binocular Eye Position in the Rostral Superior Parietal Lobule

Neural activity was recorded in area PE (dorsorostral part of Brodmanns area 5) of the posterior parietal cortex while monkeys performed arm reaching toward memorized targets located at different distances from the body. For any given distance, arm movements were performed while the animal kept binocular eye fixation constant. Under these conditions, the activity of a large proportion (36%) of neurons was modulated by reach distance during the memory period. By varying binocular eye position (vergence angle) and initial hand position, we found that the reaching-related activity of most neurons (61%) was influenced by changing the starting position of the hand, whereas that of a smaller, although substantial, population (13%) was influenced by changes of binocular eye position (i.e., by the angle of vergence). Furthermore, the modulation of the neural activity was better explained expressing the reach movement end-point, corresponding to the memorized target location, in terms of distance from the initial hand position, rather than from the body. These results suggest that the activity of neurons in area PE combines information about eye and hand position to encode target distance for reaching in depth predominantly in hand coordinates. This encoding mechanism is consistent with the position of PE in the functional gradient that characterizes the parieto-frontal network underlying reaching.

Comparison of Strategy Signals in the Dorsolateral and Orbital Prefrontal Cortex

Abstract behavior-guiding rules and strategies allow monkeys to avoid errors in rarely encountered situations. In the present study, we contrasted strategy-related neuronal activity in the dorsolateral prefrontal cortex (PFdl) and the orbital prefrontal cortex (PFo) of rhesus monkeys. On each trial of their behavioral task, the monkeys responded to a foveal visual cue by making a saccade to one of two spatial targets. One response required a leftward saccade, the other required a saccade of equal magnitude to the right. The cues instructed the monkeys to follow one of two response strategies: to stay with their most recent successful response or to shift to the alternative response. Neurons in both areas encoded the stay and shift strategies after the cue appeared, but there were three major differences between the PFo and the PFdl: (1) many strategy-encoding cells in PFdl also encoded the response (left or right), but few, if any, PFo cells did so; (2) strategy selectivity appeared earlier in PFo than in PFdl; and (3) on error trials, PFo neurons encoded the correct strategy—the one that had been cued but not implemented—whereas in PFdl the strategy signals were weak or absent on error trials. These findings indicate that PFo and PFdl both contribute to behaviors guided by abstract response strategies, but do so differently, with PFo encoding a strategy and PFdl encoding a response based on a strategy.

Neuronal Activity during a Cued Strategy Task: Comparison of Dorsolateral, Orbital, and Polar Prefrontal Cortex

We compared neuronal activity in the dorsolateral (PFdl), orbital (PFo), and polar (PFp) prefrontal cortex as monkeys performed three tasks. In two tasks, a cue instructed one of two strategies: stay with the previous response or shift to the alternative. Visual stimuli served as cues in one of these tasks; in the other, fluid rewards did so. In the third task, visuospatial cues instructed each response. A delay period followed each cue. As reported previously, PFdl encoded strategies (stay or shift) and responses (left or right) during the cue and delay periods, while PFo encoded strategies and PFp encoded neither strategies nor responses; during the feedback period, all three areas encoded responses, but not strategies. Four novel findings emerged from the present analysis. (1) The strategy encoded by PFdl and PFo cells during the cue and delay periods was modality specific. (2) The response encoded by PFdl cells was task and modality specific during the cue period, but during the delay and feedback periods it became task and modality general. (3) Although some PFdl and PFo cells responded to or anticipated rewards, we could rule out reward effects for most strategy- and response-related activity. (4) Immediately before feedback, only PFp signaled responses that were correct according to the cued strategy; after feedback, only PFo signaled the response that had been made, whether correct or incorrect. These signals support a role in generating responses by PFdl, assigning outcomes to choices by PFo, and assigning outcomes to cognitive processes by PFp.

Encoding Goals but Not Abstract Magnitude in the Primate Prefrontal Cortex

Functional neuroimaging studies show that perceptual judgments about time and space activate similar prefrontal and parietal areas, and it is known that perceptions in these two cognitive domains interfere with each other. These findings have led to the theory that temporal and spatial perceptions, among other metrics, draw on a common representation of magnitude. Our results indicate that an alternative principle applies to the prefrontal cortex. Analysis at the single-cell level shows that separate, domain-specific populations of neurons encode relative magnitude in time and space. These neurons are intermixed with each other in the prefrontal cortex, along with a separate intermixed population that encodes the goal chosen on the basis of these perceptual decisions. As a result, domain-specific neural processing at the single-cell level seems to underlie domain generality as observed at the regional level, with a common representation of prospective goals rather than a common representation of magnitude.