Formalizing planning and information search in naturalistic decision-making.

Decisions made by mammals and birds are often temporally extended. They require planning and sampling of decision-relevant information. Our understanding of such decision-making remains in its infancy compared with simpler, forced-choice paradigms. However, recent advances in algorithms supporting planning and information search provide a lens through which we can explain neural and behavioral data in these tasks. We review these advances to obtain a clearer understanding for why planning and curiosity originated in certain species but not others; how activity in the medial temporal lobe, prefrontal and cingulate cortices may support these behaviors; and how planning and information search may complement each other as means to improve future action selection.

Dynamics of hippocampal ensemble activity realignment: time versus space.

Whether hippocampal map realignment is coupled more strongly to position or time was studied in rats trained to shuttle on a linear track. The rats were required to run from a start box and to pause at a goal location at a fixed location relative to stable distal cues (room-aligned coordinate frame). The origin of each lap was varied by shifting the start box and track as a unit (box-aligned coordinate frame) along the direction of travel. As observed by Gothard et al. (1996a), on each lap the hippocampal activity realigned from a representation that was box-aligned to one that was room-aligned. We studied the dynamics of this transition using a measure of how well the moment-by-moment ensemble activity matched the expected activity given the location of the animal in each coordinate frame. The coherency ratio, defined as the ratio of the matches for the two coordinate systems, provides a quantitative measure of the ensemble activity alignment and was used to compare four possible descriptions of the realignment process. The elapsed time since leaving the box provided a better predictor of the occurrence of the transition than any of the three spatial parameters investigated, suggesting that the shift between coordinate systems is at least partially governed by a stochastic, time-dependent process.

Independence of firing correlates of anatomically proximate hippocampal pyramidal cells.

In neocortex, neighboring neurons frequently exhibit correlated encoding properties. There is conflicting evidence whether a similar phenomenon occurs in hippocampus. To assess this quantitatively, a comparison was made of the spatial and temporal firing correlations within and between local groups of hippocampal cells, spaced 350-1400 microm apart. No evidence of clustering was found in a sample of >3000 neurons. Moreover, cells active in two environments were uniformly interspersed at a scale of <100 microm, as assessed by the activity-induced gene Arc. Independence of encoding characteristics implies uncorrelated inputs, which could enhance the capacity of the hippocampus to store arbitrary associations.

Quantitative measures of cluster quality for use in extracellular recordings.

While the use of multi-channel electrodes (stereotrodes and tetrodes) has allowed for the simultaneous recording and identification of many neurons, quantitative measures of the quality of neurons in such recordings are lacking. In multi-channel recordings, each spike waveform is discriminated in a high-dimensional space, making traditional measures of unit quality inapplicable. We describe two measures of unit isolation quality, Lratio and Isolation Distance, and evaluate their performance using simulations and tetrode recordings. Both measures quantified how well separated the spikes of one cluster (putative neuron) were from other spikes recorded simultaneously on the same multi-channel electrode. In simulations and tetrode recordings, both Lratio and Isolation Distance discriminated well- and poorly-separated clusters. In data sets from the rodent hippocampus in which neurons were simultaneously recorded intracellularly and extracellularly, values of Isolation Distance and Lratio were related to the correct identification of spikes.

Measuring fundamental frequencies in local field potentials.

Neural processes display rhythmic oscillations in local field potentials; identification of their characteristic frequencies is complicated due to their highly non-stationary nature. A simple technique, combining Fourier transforms and correlation coefficients yields unambiguous determinations of the frequencies without a priori filtering. This procedure also provides quantitative information concerning interactions between frequencies. Fundamental frequencies in local field potential data acquired from the hippocampus, cortex, and striatum from awake, behaving rats were calculated using this technique. Characteristic frequencies identified using this technique from hippocampus and cortex agreed with known oscillations. Application to dorsal striatal local field potentials identified a low-frequency theta component as well as a narrow gamma band oscillation at 50-55 Hz.

The hippocampal debate: are we asking the right questions?

For years, the debate has been: "Is the hippocampus the cognitive map?" or "Is the hippocampus the core of memory?" These two hypotheses derived their original power from two key experiments--the cognitive map theory from the remarkable spatial correlates seen in recordings of hippocampal pyramidal cells and the memory theory from the profound amnesias seen in the patient H.M. Both of these key experiments have been reinterpreted over the years: hippocampal cells are correlated with much more than place and H.M. is missing much more than just his hippocampus. However, both theories are still debated today. The hippocampus clearly plays a role in both navigation and memory processing. The question that must be addressed is rather: "What is the role played by the hippocampus in the navigation and memory systems?" By looking at the navigation system as a whole, one can identify the major role played by the hippocampus as correcting for accumulation errors that occur within idiothetic navigation systems. This is most clearly experimentally evident as reorientation when an animal is lost. Carrying this over to a more general process, this becomes a role of recalling a context, bridging a contextual gap, or, in other words, it becomes a form of recognition memory. I will review recent experimental data which seems to support this theory over the more general spatial or memory theories traditionally applied to hippocampus.

Development of path stereotypy in a single day in rats on a multiple-T maze.

Humans and animals trained on sequential reaction tasks show decreases in reaction time and increases in anticipatory movements even long after they have ceased to make errors. Humans show these changes even when they do not explicitly recognize that they performed a repeating sequence. We have developed a task which rats learn to perform error-free quickly, but in which they continue to show path-refinement on a single day. This task may enable the study of performance strategy changes occurring within a single day.

Prediction, sequences and the hippocampus.

Recordings of rat hippocampal place cells have provided information about how the hippocampus retrieves memory sequences. One line of evidence has to do with phase precession, a process organized by theta and gamma oscillations. This precession can be interpreted as the cued prediction of the sequence of upcoming positions. In support of this interpretation, experiments in two-dimensional environments and on a cue-rich linear track demonstrate that many cells represent a position ahead of the animal and that this position is the same irrespective of which direction the rat is coming from. Other lines of investigation have demonstrated that such predictive processes also occur in the non-spatial domain and that retrieval can be internally or externally cued. The mechanism of sequence retrieval and the usefulness of this retrieval to guide behaviour are discussed.

Task-dependent encoding of space and events by striatal neurons is dependent on neural subtype.

The dorsal striatum plays a critical role in procedural learning and memory. Current models of basal ganglia assume that striatal neurons and circuitry are critical for the execution of overlearned, habitual sequences of action. However, less is known about how the striatum encodes task information that guides the performance of actions in procedural tasks. To explore the striatal encoding of task information, we compared the behavioral correlates of striatal neurons tested in two tasks: a multiple T-maze task in which reward delivery was entirely predictable based on spatial cues (the Multiple-T task), and a task in which rats ran on a rectangular track, but food delivery depended on the distance traveled on the track and was not dependent solely on spatial location (the Take-5 task). Striatal cells recorded on these tasks were divisible into three cell types: phasic-firing neurons (PFNs), tonically firing neurons (TFNs), and high-firing neurons (HFNs) and similar proportions of each cell type were found in each task. However, the behavioral correlates of each cell type were differentially sensitive to the type of task rats were performing. PFNs were responsive to specific task-parameters on each task. TFNs showed reliable burst-and-pause responses following food delivery and other events that were consistent with tonically active neurons (TANs) on the Take-5 (non-spatial) task but not on the Multiple-T (spatial) task. HFNs showed spatial oscillations on the Multiple-T (spatial) task but not the Take-5 (non-spatial) task. Reconstruction of the rats' position on the maze was highly accurate when using striatal ensembles recorded on the Multiple-T (spatial) task, but not when using ensembles recorded on the Take-5 (non-spatial) task. In contrast, reconstruction of time following food delivery was successful in both tasks. The results indicated a strong task dependency of the quality of the spatial, but not the reward-related, striatal representations on these tasks. These results suggest that striatal spatial representations depend on the degree to which spatial task-parameters can be unambiguously associated with goals.

A motorized microdrive for recording of neural ensembles in awake behaving rats.

The recording of neural ensembles in awake, behaving rats has been an extremely successful experimental paradigm, providing demonstrable scientific advances. Dynamic control of the position of the implanted electrodes is of key importance as mobile electrodes provide a better signal-to-noise ratio and a better cell/ electrode yield than nonmobile electrodes. Here we describe the use of low cost, soon to be commercially available dc motors to successfully control the depth of electrodes. The prototype designed is approximately 30 mm in diameter and 50 mm in length and weighed about 30 gms. This paper presents the results of linear displacements of electrodes achievable with this motorized microdrive.

Theory of rodent navigation based on interacting representations of space.

We present a computational theory of navigation in rodents based on interacting representations of place, head direction, and local view. An associated computer model is able to replicate a variety of behavioral and neurophysiological results from the rodent navigation literature. The theory and model generate predictions that are testable with current technologies.

The reaching task: evidence for vector arithmetic in the motor system?

During a reaching task, the population vector is an encoding of direction based on cells with cosine response functions. Scaling the response by a magnitude factor produces a vector encoding, enabling vector arithmetic to be performed by the summation of firing rates. We show that the response properties of selected populations of cells in the primary motor cortex and area 5 can be explained in terms of arithmetic relationships among load, goal, and motor command vectors. Our computer simulations show good agreement with single-cell recording data.

The role of the hippocampus in solving the Morris water maze.

We suggest that the hippocampus plays two roles that allow rodents to solve the hidden-platform water maze: self-localization and route replay. When an animal explores an environment such as the water maze, the combination of place fields and correlational (Hebbian) long-term potentiation produces a weight matrix in the CA3 recurrent collaterals such that cells with overlapping place fields are more strongly interconnected than cells with nonoverlapping fields. When combined with global inhibition, this forms an attractor with coherent representations of position as stable states. When biased by local view information, this allows the animal to determine its position relative to the goal when it returns to the environment. We call this self-localization. When an animal traces specific routes within an environment, the weights in the CA3 recurrent collaterals become asymmetric. We show that this stores these routes in the recurrent collaterals. When primed with noise in the absence of sensory input, a coherent representation of position still forms in the CA3 population, but then that representation drifts, retracing a route. We show that these two mechanisms can coexist and form a basis for memory consolidation, explaining the anterograde and limited retrograde amnesia seen following hippocampal lesions.

Cognitive maps beyond the hippocampus.

We present a conceptual framework for the role of the hippocampus and its afferent and efferent structures in rodent navigation. Our proposal is compatible with the behavioral, neurophysiological, anatomical, and neuropharmacological literature, and suggests a number of practical experiments that could support or refute it. We begin with a review of place cells and how the place code for an environment might be aligned with sensory cues and updated by self-motion information. The existence of place fields in the dark suggests that location information is maintained by path integration, which requires an internal representation of direction of motion. This leads to a consideration of the organization of the rodent head direction system, and thence into a discussion of the computational structure and anatomical locus of the path integrator. If the place code is used in navigation, there must be a mechanism for selecting an action based on this information. We review evidence that the nucleus accumbens subserves this function. From there, we move to interactions between the hippocampal system and the environment, emphasizing mechanisms for learning novel environments and for aligning the various subsystems upon re-entry into familiar environments. We conclude with a discussion of the relationship between navigation and declarative memory.