How Laminar Frontal Cortex and Basal Ganglia Circuits Interact to Control Planned and Reactive Saccades

The basal ganglia and frontal cortex together allow animals to learn adaptive responses that acquire rewards when prepotent reflexive responses are insufficient. Anatomical studies show a rich pattern of interactions between the basal ganglia and distinct frontal cortical layers. Analysis of the laminar circuitry of the frontal cortex, together with its interactions with the basal ganglia, motor thalamus, superior colliculus, and inferotemporal and parietal cortices, provides new insight into how these brain regions interact to learn and perform complexly conditioned behaviors. A neural model whose cortical component represents the frontal eye fields captures these interacting circuits. Simulations of the neural model illustrate how it provides a functional explanation of the dynamics of 17 physiologically identified cell types found in these areas. The model predicts how action planning or priming (in cortical layers III and VI) is dissociated from execution (in layer V), how a cue may serve either as a movement target or as a discriminative cue to move elsewhere, and how the basal ganglia help choose among competing actions. The model simulates neurophysiological, anatomical, and behavioral data about how monkeys perform saccadic eye movement tasks, including fixation; single saccade, overlap, gap, and memory-guided saccades; anti-saccades; and parallel search among distractors.Defense Advanced Research Projects Agency and the Office of Naval Research (N00014-95-l-0409, N00014-92-J-1309, N00014-95-1-0657); National Science Foundation (IRI-97-20333)

Primate pre-arcuate cortex actively maintains persistent representations of saccades from plans to outcomes

Dorso-lateral prefrontal cortex is thought to contribute to adaptive behavior by integrating temporally dispersed, behaviorally-relevant factors. Past work has revealed a variety of neural representations preceding actions, which are involved in internal processes like planning, working memory and covert attention. Task-related activity following actions has often been reported, but so far lacks a clear interpretation. We leveraged modified versions of classic oculomotor paradigms and population recordings to show that post-saccadic activity is a dominant signal in dorso-lateral prefrontal cortex that is distinct from pre-saccadic activity. Unlike pre-saccadic activity, post-saccadic activity occurs after each saccade, although its strength and duration are modulated by task context and expected rewards. In contrast to representations preceding actions, which appear to be mixed randomly across neurons, post-saccadic activity results in representations that are highly structured at the single-neuron and population level. Overall, the properties of post-saccadic activity are consistent with those of an action memory, an internal process with a possible role in learning and updating spatial representations

Multimodal Representation of Space in the Posterior Parietal Cortex and its use in Planning Movements

Recent experiments are reviewed that indicate that sensory signals from many modalities, as well as efference copy signals from motor structures, converge in the posterior parietal cortex in order to code the spatial locations of goals for movement. These signals are combined using a specific gain mechanism that enables the different coordinate frames of the various input signals to be combined into common, distributed spatial representations. These distributed representations can be used to convert the sensory locations of stimuli into the appropriate motor coordinates required for making directed movements. Within these spatial representations of the posterior parietal cortex are neural activities related to higher cognitive functions, including attention. We review recent studies showing that the encoding of intentions to make movements is also among the cognitive functions of this area

Temporal structure in neuronal activity during working memory in Macaque parietal cortex

A number of cortical structures are reported to have elevated single unit firing rates sustained throughout the memory period of a working memory task. How the nervous system forms and maintains these memories is unknown but reverberating neuronal network activity is thought to be important. We studied the temporal structure of single unit (SU) activity and simultaneously recorded local field potential (LFP) activity from area LIP in the inferior parietal lobe of two awake macaques during a memory-saccade task. Using multitaper techniques for spectral analysis, which play an important role in obtaining the present results, we find elevations in spectral power in a 50--90 Hz (gamma) frequency band during the memory period in both SU and LFP activity. The activity is tuned to the direction of the saccade providing evidence for temporal structure that codes for movement plans during working memory. We also find SU and LFP activity are coherent during the memory period in the 50--90 Hz gamma band and no consistent relation is present during simple fixation. Finally, we find organized LFP activity in a 15--25 Hz frequency band that may be related to movement execution and preparatory aspects of the task. Neuronal activity could be used to control a neural prosthesis but SU activity can be hard to isolate with cortical implants. As the LFP is easier to acquire than SU activity, our finding of rich temporal structure in LFP activity related to movement planning and execution may accelerate the development of this medical application.Comment: Originally submitted to the neuro-sys archive which was never publicly announced (was 0005002

Change blindness: eradication of gestalt strategies

Arrays of eight, texture-defined rectangles were used as stimuli in a one-shot change blindness (CB) task where there was a 50% chance that one rectangle would change orientation between two successive presentations separated by an interval. CB was eliminated by cueing the target rectangle in the first stimulus, reduced by cueing in the interval and unaffected by cueing in the second presentation. This supports the idea that a representation was formed that persisted through the interval before being 'overwritten' by the second presentation (Landman et al, 2003 Vision Research 43149–164]. Another possibility is that participants used some kind of grouping or Gestalt strategy. To test this we changed the spatial position of the rectangles in the second presentation by shifting them along imaginary spokes (by ±1 degree) emanating from the central fixation point. There was no significant difference seen in performance between this and the standard task [F(1,4)=2.565, p=0.185]. This may suggest two things: (i) Gestalt grouping is not used as a strategy in these tasks, and (ii) it gives further weight to the argument that objects may be stored and retrieved from a pre-attentional store during this task

Decoding motor intentions from human brain activity

“You read my mind.” Although this simple everyday expression implies ‘knowledge or understanding’ of another’s thinking, true ‘mind-reading’ capabilities implicitly seem constrained to the domains of Hollywood and science-fiction. In the field of sensorimotor neuroscience, however, significant progress in this area has come from mapping characteristic changes in brain activity that occur prior to an action being initiated. For instance, invasive neural recordings in non-human primates have significantly increased our understanding of how highly cognitive and abstract processes like intentions and decisions are represented in the brain by showing that it is possible to decode or ‘predict’ upcoming sensorimotor behaviors (e.g., movements of the arm/eyes) based on preceding changes in the neuronal output of parieto-frontal cortex, a network of areas critical for motor planning. In the human brain, however, a successful counterpart for this predictive ability and a similar detailed understanding of intention-related signals in parieto-frontal cortex have remained largely unattainable due to the limitations of non-invasive brain mapping techniques like functional magnetic resonance imaging (fMRI). Knowing how and where in the human brain intentions or plans for action are coded is not only important for understanding the neuroanatomical organization and cortical mechanisms that govern goal-directed behaviours like reaching, grasping and looking – movements critical to our interactions with the world – but also for understanding homologies between human and non-human primate brain areas, allowing the transfer of neural findings between species. In the current thesis, I employed multi-voxel pattern analysis (MVPA), a new fMRI technique that has made it possible to examine the coding of neural information at a more fine-grained level than that previously available. I used fMRI MVPA to examine how and where movement intentions are coded in human parieto-frontal cortex and specifically asked the question: What types of predictive information about a subject\u27s upcoming movement can be decoded from preceding changes in neural activity? Project 1 first used fMRI MVPA to determine, largely as a proof-of-concept, whether or not specific object-directed hand actions (grasps and reaches) could be predicted from intention-related brain activity patterns. Next, Project 2 examined whether effector-specific (arm vs. eye) movement plans along with their intended directions (left vs. right) could also be decoded prior to movement. Lastly, Project 3 examined exactly where in the human brain higher-level movement goals were represented independently from how those goals were to be implemented. To this aim, Project 3 had subjects either grasp or reach toward an object (two different motor goals) using either their hand or a novel tool (with kinematics opposite to those of the hand). In this way, the goal of the action (grasping vs. reaching) could be maintained across actions, but the way in which those actions were kinematically achieved changed in accordance with the effector (hand or tool). All three projects employed a similar event-related delayed-movement fMRI paradigm that separated in time planning and execution neural responses, allowing us to isolate the preparatory patterns of brain activity that form prior to movement. Project 1 found that the plan-related activity patterns in several parieto-frontal brain regions were predictive of different upcoming hand movements (grasps vs. reaches). Moreover, we found that several parieto-frontal brain regions, similar to that only previously demonstrated in non-human primates, could actually be characterized according to the types of movements they can decode. Project 2 found a variety of functional subdivisions: some parieto-frontal areas discriminated movement plans for the different reach directions, some for the different eye movement directions, and a few areas accurately predicted upcoming directional movements for both the hand and eye. This latter finding demonstrates -- similar to that shown previously in non-human primates -- that some brain areas code for the end motor goal (i.e., target location) independent of effector used. Project 3 identified regions that decoded upcoming hand actions only, upcoming tool actions only, and rather interestingly, areas that predicted actions with both effectors (hand and tool). Notably, some of these latter areas were found to represent the higher-level goals of the movement (grasping vs. reaching) instead of the specific lower-level kinematics (hand vs. tool) necessary to implement those goals. Taken together, these findings offer substantial new insights into the types of intention-related signals contained in human brain activity patterns and specify a hierarchical neural architecture spanning parieto-frontal cortex that guides the construction of complex object-directed behaviors