We study the impact of correlated neuronal firing rate variability on the accuracy with which an encoded quantity can be extracted from a population of neurons. Contrary to a widespread belief, correlations in the variabilities of neuronal firing rates do not, in general, limit the increase in coding accuracy provided by using large populations of encoding neurons. Furthermore, in some cases, but not all, correlations improve the accuracy of a population code.

The problem of predicting the position of a freely foraging rat based on the ensemble firing patterns of place cells recorded from the CA1 region of its hippocampus is used to develop a two-stage statistical paradigm for neural spike train decoding. In the first,or encoding stage,place cell spiking activity is modeled as an inhomogeneous Poisson process whose instantaneous rate is a function of the animal’s position in space and phase of its theta rhythm. The animal’s path is modeled as a Gaussian random walk. In the second,or decoding stage,a Bayesian statistical paradigm is used to derive a nonlinear recursive causal filter algorithm for predicting the position of the animal from the place cell ensemble firing patterns. The algebra of the decoding algorithm defines an explicit map of the discrete spike trains into the position prediction. The confidence regions for the position predictions quantify spike train infor-

such as the orientation of a line in the visual field or the location of Two main goals for reconstruction are approached in this the body in space are coded as activity levels in populations of neurons. Reconstruction or decoding is an inverse problem in which paper. The first goal is technical and is exemplified by the the physical variables are estimated from observed neural activity. population vector method applied to motor cortical activities Reconstruction is useful first in quantifying how much information during various reaching tasks (Georgopoulos et al. 1986, 1989; about the physical variables is present in the population and, second, Schwartz 1994) and the template matching method applied to in providing insight into how the brain might use distributed represen- disparity selective cells in the visual cortex (Lehky and Sejnowtations in solving related computational problems such as visual ob- ski 1990) and hippocampal place cells during rapid learning of ject recognition and spatial navigation. Two classes of reconstruction place fields in a novel environment (Wilson and McNaughton methods, namely, probabilistic or Bayesian methods and basis func- 1993). In these examples, reconstruction extracts information tion methods, are discussed. They include important existing methods from noisy neuronal population activity and transforms it to a

During sensory-guided motor tasks, information must be transferred from arrays of neurons coding target location to motor networks that generate and control movement. We address two basic questions about this information transfer. First, what mechanisms assure that the different neural representations align properly so that activity in the sensory network representing target location evokes a motor response generating accurate movement toward the target? Coordinate transformations may be needed to put the sensory data into a form appropriate for use by the motor system. For example, in visually guided reaching the location of a target relative to the body is determined by a combination of the position of its image on the retina and the direction of gaze. What assures that the motor network responds to the appropriate combination of sensory inputs corresponding to target position in body- or arm-centered coordinates ? To answer these questions, we model a sensory network coding target p...

We present a general encoding-decoding framework for interpreting the activity of a population of units. A standard population code interpretation method, the Poisson model, starts from a description as to how a single value of an underlying quantity can generate the activities of each unit in the population. In casting it in the encoding-decoding framework, we find that this model is too restrictive to describe fully the activities of units in population codes in higher processing areas, such as the medial temporal area. Under a more powerful model, the population activity can convey information not only about a single value of some quantity but also about its whole distribution, including its variance, and perhaps even the certainty the system has in the actual presence in the world of the entity generating this quantity. We propose a novel method for forming such probabilistic interpretations of population codes and compare it to the existing method.

. A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learnin...

Coarse codes are widely used throughout the brain to encode sensory and motor variables. Methods designed to interpret these codes, such as population vector analysis, are either inefficient (the variance of the estimate is much larger than the smallest possible variance) or biologically implausible, like maximum likelihood. Moreover, these methods attempt to compute a scalar or vector estimate of the encoded variable. Neurons are faced with a similar estimation problem. They must read out the responses of the presynaptic neurons, but, by contrast, they typically encode the variable with a further population code rather than as a scalar. We show how a nonlinear recurrent network can be used to perform estimation in a near-optimal way while keeping the estimate in a coarse code format. This work suggests that lateral connections in the cortex may be involved in cleaning up uncorrelated noise among neurons representing similar variables.

Using experimental facts about long-term potentiation (LTP) and hippocampal place cells, we model how a spatial map of the environment can be created in the rat hippocampus. Sequential firing of place cells during exploration induces, in the model, a pattern of LTP between place cells that shifts the location coded by their ensemble activity away from the actual location of the animal. These shifts provide a navigational map that, in a simulation of the Morris maze, can guide the animal toward its goal. The model demonstrates how behaviorally generated modifications of synaptic strengths can be read out to affect subsequent behavior. Our results also suggest a way that navigational maps can be constructed from experimental recordings of hippocampal place cells. *Current address: Dept. of Brain and Cognitive Sciences, MIT E25-236, 45 Carlton St., Cambridge, MA 02139. Blockade of long term potentiation (LTP) and hippocampal lesions drastically impair

We analyze a model of navigational map formation based on correlation-based, temporally asymmetric potentiation and depression of synapses between hippocampal place cells. We show that synaptic modification during random exploration of an environment shifts the location encoded by place cell activity in such a way that it indicates the direction from any location to a fixed target avoiding walls and other obstacles. Multiple maps to different targets can be simultaneously stored if we introduce target-dependent modulation of place cell activity. Once maps to a number of target locations in a given environment have been stored, novel maps to previously unknown target locations are automatically constructed by interpolation between existing maps.

Population coding, where neurons with broad and overlapping firing rate tuning curves collectively encode information about a stimulus, is a common feature of sensory systems.We use decoding methods and measured properties of NMDA-mediated LTP induction to study the impact of long-term potentiation of synapses between the neurons of such a coding array. We find that, due to a temporal asymmetry in the induction of NMDA-mediated LTP, firing patterns in a neuronal array that initially represent the current value of a sensory input will, after training, provide an experienced-based prediction of that input instead. We compute how this prediction arises from and depends on the training experience. We also show how the encoded prediction can be used to generate learned motor sequences, such as the movement of a limb. This involves a novel form of memory recall that is driven by the motor response so that it automatically generates new information at a rate appropriate for the task being per...