Scientific Understanding of Consciousness
Parietal Cortex Decision-Making
Nature 484, 42–43 (05 April 2012)
Parietal Cortex Orchestrates Decision-Making As Highly Organized Sequences of Short-Lived Neuronal Activity
Eduardo Dias-Ferreira & Rui M. Costa
Champalimaud Neuroscience Programme, Champalimaud Center for the Unknown, Lisbon, Portugal.
Decision-specific sequences of neuronal activity in the parietal cortex of mice during a memory-guided navigation task were not signalled by sustained activity of particular neurons during the decision-making period, as has been shown in other studies. Rather, the choice was indicated by the activation of specific sequences of intermingled neuronal populations, with each neuron transiently active during a particular period of the task.
The researchers used a virtual T-shaped maze that mice, with their heads restrained, explored by running on a spherical treadmill. At the same time, the authors tracked the activity of individual neurons in a specific layer of the animals' parietal cortex by imaging cellular calcium levels — an indication of neuronal activity — using two-photon microscopy. In each trial, the mouse would actively navigate through a first part of the maze, where a visual cue would be presented. After that, there was a delay period in which it would continue straight ahead until it faced a crossroad where, depending on the initial cue, it had to take either a left or a right turn to reach a reward.
The authors recorded the activity of sufficient numbers of neurons simultaneously to notice that neurons with sustained activity during an entire task period (cue, delay or decision) were rare. Moreover, the choice made by the mouse — left or right turn — could be predicted at any point in the maze from a sparse pattern of the neuronal activity at the ensemble level. From a bird's-eye view, these activation patterns showed an ordered progression through specific neuronal populations, reflecting not merely the spatial and temporal progression of the mouse through the maze, but its future choice.
Neurons with sustained activity were observed rarely in these experiments.
The choice-specific sequential activation of neurons along the maze probably reflects the emergence of functional motifs for action planning.
Choice-specific functional motifs are intermingled: there was no apparent local organization of neurons tuned for specific task periods or for specific choice preferences.
There is a growing body of evidence for anatomically intermixed functional motifs.
It has been found that intermingled circuits can implement functional connectivity. In fact, these researchers provide indirect evidence that supports the emergence of functionally connected neuronal assemblies, much like those proposed by Donald Hebb in the 1940s, given that neurons that are sequentially activated during correctly performed trials have similar activity relationships during incorrectly performed trials and inter-trial intervals. This observation raises the possibility that — as has been observed in other neuronal circuits — the sequential activation of neurons in the parietal cortex emerges from internal dynamics, probably reflecting the connectivity patterns in the circuit.
Accumulated evidence from studies in various animals — from leeches to songbirds and rodents — points towards sequence-based dynamics as a common mechanism underlying action planning. The ordered progression of neuronal activity through a population of neurons suggests that indexing of information or time coordination occurs as an action is being performed. Consequently, different actions might be established as competition between different paths of activity at the neural-circuit level. According to this view, particular environmental features would trigger sequences of neuronal activity that would lead to specific actions depending on the functional connectivity between sequence elements.
The parietal cortex is interconnected with other brain areas involved in, for example, sensory and motor processing, memory and decision-making. Such a strategic position, together with the neuronal-population dynamics places the parietal cortex at the heart of the competition leading to specific actions.
[end of paraphrase]
Nature 484, 62–68 (05 April 2012)
Choice-specific sequences in parietal cortex during a virtual-navigation decision task
Christopher D. Harvey, Philip Coen1, & David W. Tank
Bezos Center for Neural Circuit Dynamics, Princeton University, Princeton, New Jersey 08544, USA
Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA
Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA
Present address: Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, USA.
The posterior parietal cortex (PPC) has an important role in many cognitive behaviours; however, the neural circuit dynamics underlying PPC function are not well understood. Here we optically imaged the spatial and temporal activity patterns of neuronal populations in mice performing a PPC-dependent task that combined a perceptual decision and memory-guided navigation in a virtual environment. Individual neurons had transient activation staggered relative to one another in time, forming a sequence of neuronal activation spanning the entire length of a task trial. Distinct sequences of neurons were triggered on trials with opposite behavioural choices and defined divergent, choice-specific trajectories through a state space of neuronal population activity. Cells participating in the different sequences and at distinct time points in the task were anatomically intermixed over microcircuit length scales (<100 micrometres). During working memory decision tasks, the PPC may therefore perform computations through sequence-based circuit dynamics, rather than long-lived stable states, implemented using anatomically intermingled microcircuits.
In real-world tasks, decision-making and working memory often occur in the context of other complex behaviours, including spatial navigation. For example, when driving through a city towards a destination, sensory information defining context and place engages memory and decision circuits to plan turns at upcoming intersections. The PPC is a prime candidate for the neuronal circuitry combining the cognitive processing elements necessary for such tasks. In primates, the PPC is important for perceptual decision-making and categorization, movement planning, and spatial attention. Studies in rats suggest that the PPC is also important for encoding route progression during navigation. Using a virtual-reality system for mice and cellular resolution optical imaging methods we developed a T-maze-based navigation task combining all these cognitive elements and characterized the neuronal circuit dynamics in the PPC, which have not been studied in this combined behavioural context.
Neuronal activity patterns in the PPC have been studied using microelectrode recordings during spatial attention, working memory and perceptual decision tasks. These studies have commonly found cells with sustained firing rate changes spanning entire task periods (cue, delay, response periods).
We explored whether PPC dynamics are best described in terms of cell classes or high-dimensional dynamics. Exploiting the ability of cellular resolution optical measurements to provide the relative anatomical location of the recorded cells, we found that neurons active during behaviourally distinct task periods and on trials with different behavioural choices were spatially intermixed over microcircuit length scales.
Because the location of the mouse PPC has not been characterized, we first performed retrograde and anterograde labelling experiments to locate it anatomically. We identified a region consistent with the rat and primate PPC based on the set of areas from where it received axonal projections, the areas to which it sent projections, and its location relative to other cortical regions.
We used two-photon microscopy to image layer 2/3 PPC neurons expressing the genetically encoded calcium indicator GCaMP3, which increases in fluorescence intensity in response to action potential firing. On average, we imaged ~65 cells simultaneously within an area ~300 µm by ~150 µm (range, 37–94 cells). Nearly all imaged cells showed statistically significant Ca2+ transients during the behavioural session. These task-modulated cells had Ca2+ transients for only short time intervals on individual trials, such that only a small fraction of neurons was active simultaneously. Cells with prolonged activity patterns covering a large fraction of the trial were not observed. The majority (~71%) of task-modulated cells had significantly different levels of activity on correct right and left choice trials (choice-specific cells). Similar choice-specific, task-modulated activity patterns were observed in extracellular electrophysiological recordings. Cells were also active on error trials, such that neurons active during the cue period tended to be correlated with the cue identity, and neurons active during the turn period in general were correlated with the behavioural response. Only a small fraction of cells had obvious reward-related signals (~2% of active cells with P < 0.01, t-test, comparing ΔF/F values within ~0.6 s after the reward was given on correct trials or missed on error trials).
When the activity patterns of all the choice-specific, task-modulated cells were ordered according to the time profile of their Ca2+ transients, the active periods across cells were staggered relative to one another in time, forming a sequence of neuronal activation covering the entire trial length.
Because previous studies of the PPC have categorized cells into classes with cue, delay or response period activity, we examined the activity patterns to see if neurons in the sequence were grouped on the basis of behavioural periods. Consistently, principal component analysis (PCA) of the mean ΔF/F traces for all cells revealed three intermixed groups, with each group mostly containing cells preferring the same behavioural period.
Although the population of neurons could be divided into groups, the temporal activity patterns within each individual period were heterogeneous and formed sequences. Cells within their preferred period were active for only a fraction of the period (35 ± 16% of time points in preferred periods with a Ca2+ transient), with different cells active at different times.
Together these data indicate that classes of cells with homogeneous activity patterns were not present. Rather, choice-specific sequences of neurons were activated in all behavioural periods, with a lower density of cells in the sequence at the borders between periods.
The heterogeneous and sequential neuronal activity patterns during the T-maze task indicated that we should consider the dynamics of the population rather than classes of cells. We therefore analysed the dynamics as a trajectory through a state space of neuronal population activity (neuronal circuit trajectory).
Trajectories were highly variable on error trials. Some trajectories began close to the correct choice trajectory during the cue period and transitioned towards the error choice trajectory later in the trial; such transitions occurred at a wide range of points in the trial.
The choice-specific sequences of PPC neuronal activation we report here add to the growing list of studies that have identified cortical sequences of activity states during working memory tasks.
Our results also offer a way to unite previous work on neural coding in the PPC. Navigation, memory and choice information may be combined in the sequences such that the identity of the active sequence reflects choice-related information for working memory and movement planning.
Because cells that were active at distinct time points in the task and that participated in different choice-specific sequences were spatially intermingled, our results indicate that functionally distinct subnetworks are anatomically interlaced in the PPC. This extends previous work in sensory cortex, motor cortex and the hippocampus showing spatial intermixing of heterogeneous response properties in cells encoding qualitatively similar types of information or in cells with activity during similar task epochs.
Our results motivate consideration of a conceptual framework for decision-making and working memory in which sensory information used for the decision activates a neuronal sequence of activity. The sequence begins in a choice-independent state, which could be mediated by neurons that are not choice-specific, and then moves towards a choice-specific trajectory and away from other trajectories in a manner dependent on the incoming information. A decision is proposed to be reached when the sequence of activity intersects a choice-specific trajectory; different decisions involve intersections with different trajectories. Upon reaching a decision, a working memory can be maintained by continuing along that choice-specific trajectory. Changing decisions would occur through transitions between trajectories, but as time progresses in the task, the state space distance between trajectories increases, in effect creating a larger barrier to change. In this view, decision-making and working memory utilize an ordered progression through a sequence in which information moves from one population of neurons to another over time.
[end of paraphrase]
Return to — Perception-Action Cycle