Abstract Context Representations in Primate Amygdala and Prefrontal Cortex.

Neurons in prefrontal cortex (PFC) encode rules, goals, and other abstract information thought to underlie cognitive, emotional, and behavioral flexibility. Here we show that the amygdala, a brain area traditionally thought to mediate emotions, also encodes abstract information that could underlie this flexibility. Monkeys performed a task in which stimulus-reinforcement contingencies varied between two sets of associations, each defining a context. Reinforcement prediction required identifying a stimulus and knowing the current context. Behavioral evidence indicated that monkeys utilized this information to perform inference and adjust their behavior. Neural representations in both amygdala and PFC reflected the linked sets of associations implicitly defining each context, a process requiring a level of abstraction characteristic of cognitive operations. Surprisingly, when errors were made, the context signal weakened substantially in the amygdala. These data emphasize the importance of maintaining abstract cognitive information in the amygdala to support flexible behavior.

Neural mechanisms for forming a perceptual decision.

Cognitive and behavioral responses to environmental stimuli depend on an evaluation of sensory signals within the cerebral cortex. The mechanism by which this occurs in a specific visual task was investigated with a combination of physiological and psychophysical techniques. Rhesus monkeys discriminated among eight possible directions of motion while directional signals were manipulated in visual area MT. One directional signal was generated by a visual stimulus and a second signal was introduced by electrically stimulating neurons that encoded a specific direction of motion. The decisions made by the monkeys in response to the two signals allowed a distinction to be made between two possible mechanisms for interpreting directional signals in MT. The monkeys tended to cast decisions in favor of one or the other signal, indicating that the signals exerted independent effects on performance and that an interactive mechanism such as vector averaging of the two signals was not operative. Thus, the data suggest a mechanism in which monkeys chose the direction encoded by the largest signal in the representation of motion direction, a "winner-take-all" decision process.

Microstimulation in visual area MT: effects of varying pulse amplitude and frequency.

We have previously shown that perceptual judgements of motion direction are based in part on the activity of direction selective neurons in extrastriate visual area MT (Salzman et al., 1990, 1992). In those experiments, we applied low-amplitude microstimulation pulses (10 microA, 200 Hz) to clusters of MT neurons whose preferred directions were similar. The effect of microstimulation was to bias the monkeys' choices on a direction discrimination task toward the preferred direction of neurons at the stimulation site. The results suggest that microstimulation generated a directionally specific cortical signal by activating selectively neurons near the electrode tip. To test this notion more directly, we have now examined the behavioral effects of varying current amplitude, current frequency, and electrode position. In the majority of experiments, the directional bias in the monkeys' choices was reduced or eliminated as current amplitude increased to 80 microA. In addition, 80 microA stimulating pulses frequently impaired overall performance as measured by the percentage of correct responses. This decrement in performance indicated that 80 microA pulses introduced "noise" into the neural circuitry encoding motion direction, presumably by increasing current spread to activate a larger population of neurons representing all directions of motion. In contrast, increasing current frequency to 500 Hz (10 microA pulses) preserved the directional specificity of microstimulation effects. The precise position of the stimulating electrode also influenced the magnitude of microstimulation effects; in some cases, differences in position on the order of 100 microns determined whether an experiment yielded a very large effect or no effect at all. Thus, directionally specific activation of cortical circuitry within MT can be disrupted by increases in current spread or by small changes in electrode position. These observations suggest that the effects of low-amplitude microstimulation depend upon direct activation of a well-localized population of neurons.

The neuronal basis of motion perception.

The central nervous system of humans supports a range of cognitive functions that contribute to conscious mental states. The neural systems underlying several of these cognitive functions, including perception, memory, planning and action, are proving susceptible to experimental analysis in lower primate species such as rhesus monkeys. In particular, recent investigations have generated striking new insights concerning the neural mechanisms that mediate visual perception. We briefly review the functional organization of the primate visual pathways and describe new experiments that demonstrate a causal link between neural activity in one of these pathways and a specific aspect of perceptual performance. The experiments illustrate an incisive method for linking perceptual abilities to their neural substrates. This approach may prove applicable to the analysis of other cognitive functions as well.

Microstimulation in visual area MT: effects on direction discrimination performance.

Physiological and behavioral evidence suggests that the activity of direction selective neurons in visual cortex underlies the perception of moving visual stimuli. We tested this hypothesis by measuring the effects of cortical microstimulation on perceptual judgements of motion direction. To accomplish this, rhesus monkeys were trained to discriminate the direction of motion in a near-threshold, stochastic motion display. For each experiment, we positioned a microelectrode in the middle of a cluster of neurons that shared a common preferred direction of motion. The psychophysical task was then adjusted so that the visual display was presented directly over the neurons' receptive field. The monkeys were required to discriminate between motion shown either in the direction preferred by the neurons or in the opposite direction. On half the trials of an experiment, we applied electrical microstimulation while monkeys viewed the motion display. We hypothesized that enhancing the neurons' discharge rate would introduce a directionally specific signal into the cortex and thereby influence the monkeys' choices on the discrimination task. We compared the monkeys' performance on "stimulated" and "nonstimulated" trials in 139 experiments; all trials within an experiment were presented in random order. Statistically significant effects of microstimulation were obtained in 89 experiments. In 86 of the 89 experiments with significant effects (97%), the monkeys indicated that motion was in the neurons' preferred direction more frequently on stimulated trials than on nonstimulated trials. The data demonstrate a functional link between the activity of direction selective neurons and perceptual judgements of motion direction.

Cortical microstimulation influences perceptual judgements of motion direction.

Neurons in the visual cortex respond selectively to perceptually salient features of the visual scene, such as the direction and speed of moving objects, the orientation of local contours, or the colour or relative depth of a visual pattern. It is commonly assumed that the brain constructs its percept of the visual scene from information encoded in the selective responses of such neurons. We have now tested this hypothesis directly by measuring the effect on psychophysical performance of modifying the firing rates of physiologically characterized neurons. We required rhesus monkeys to report the direction of motion in a visual display while we electrically stimulated clusters of directionally selective neurons in the middle temporal visual area (MT, or V5), an extrastriate area that plays a prominent role in the analysis of visual motion information. Microstimulation biased the animals' judgements towards the direction of motion encoded by the stimulated neurons. This result indicates that physiological properties measured at the neuronal level can be causally related to a specific aspect of perceptual performance.