Populations of hippocampal neurons were recorded simultaneously in rats shuttling on a track between a fixed reward site at one end and a movable reward site, mounted in a sliding box, at the opposite end. While the rat ran toward the fixed site, the box was moved. The rat returned to the box in its new position. On the initial part of all journeys, cells fired at fixed distances from the origin, whereas on the final part, cells fired at fixed distances from the destination. Thus, on outward journeys from the box, with the box behind the rat, the position representation must have been updated by path integration. Farther along the journey, the place field map became aligned on the basis of external stimuli. The spatial representation was quantified in terms of population vectors. During shortened journeys, the vector shifted from an alignment with the origin to an alignment with the destination. The dynamics depended on the degree of mismatch with respect to the full-length journey. For small mismatches, the vector moved smoothly through intervening coordinates until the mismatch was corrected. For large mismatches, it jumped abruptly to the new coordinate. Thus, when mismatches occur, path integration and external cues interact competitively to control place-cell firing.When the same box was used in a different environment, it controlled the alignment of a different set of place cells. These data suggest that although map alignment can be controlled by landmarks, hippocampal neurons do not explicitly represent objects or events.

The behavioral correlates of rat hippocampal CA1 cells were examined in a spatial navigation task in which two cylindrical landmarks predicted the location of food. The landmarks were maintained at a constant distance from each other but were moved from trial to trial within a large arena surrounded by static background cues. On each trial, the rats were released from a box to which they returned for additional food after locating the goal. The box also was located variably from trial to trial and was moved to a new location while the animals were searching for the goal site. The discharge characteristics of multiple, simultaneously recorded cells were examined with respect to the landmarks, the static background cues, and the box in which each trial started and ended. Three clear categories of cells were observed: (1) cells with location-specific firing (place cells); (2) goal/landmark-related cells that fired in the vicinity of the goal or landmarks, regardless of their location in the arena; and (3) box-related cells that fired either when the rat was in the box or as it was leaving or entering the box, regardless of its location in the arena. Disjunctive cells with separate firing fields in more than one reference frame also were observed. These results suggest that in this task a subpopulation of hippocampal cells encodes location in the fixed spatial frame, whereas other subpopulations encode location with respect to different reference frames associated with the task-relevant, mobile objects.

Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG. Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97: 1671-1683, 2007. First published November 8, 2006 doi:10.1152/jn.00714.2006. The amygdala is purported to play an important role in face processing, yet the specificity of its activation to face stimuli and the relative contribution of identity and expression to its activation are unknown. In the current study, neural activity in the amygdala was recorded as monkeys passively viewed images of monkey faces, human faces, and objects on a computer monitor. Comparable proportions of neurons responded selectively to images from each category. Neural responses to monkey faces were further examined to determine whether face identity or facial expression drove the face-selective responses. The majority of these neurons (64%) responded both to identity and facial expression, suggesting that these parameters are processed jointly in the amygdala. Large fractions of neurons, however, showed pure identityselective or expression-selective responses. Neurons were selective for a particular facial expression by either increasing or decreasing their firing rate compared with the firing rates elicited by the other expressions. Responses to appeasing faces were often marked by significant decreases of firing rates, whereas responses to threatening faces were strongly associated with increased firing rate. Thus global activation in the amygdala might be larger to threatening faces than to neutral or appeasing faces.

The social behavior of both human and nonhuman primates relies on specializations for the recognition of individuals, their facial expressions, and their direction of gaze. A broad network of cortical and subcortical structures has been implicated in face processing, yet it is unclear whether co-occurring dimensions of face stimuli, such as expression and direction of gaze, are processed jointly or independently by anatomically and functionally segregated neural structures. Awake macaques were presented with a set of monkey faces displaying aggressive, neutral, and appeasing expressions with head and eyes either averted or directed. BOLD responses to these faces as compared to Fourier-phase-scrambled images revealed widespread activation of the superior temporal sulcus and inferotemporal cortex and included activity in the amygdala. The different dimensions of the face stimuli elicited distinct activation patterns among the amygdaloid nuclei. The basolateral amygdala, including the lateral, basal, and accessory basal nuclei, produced a stronger response for threatening than appeasing expressions. The central nucleus and bed nucleus of the stria terminalis responded more to averted than directed-gaze faces. Independent behavioral measures confirmed that faces with averted gaze were more arousing, suggesting the activity in the central nucleus may be related to attention and arousal.

Self-motion signals are sufficient for animal navigation ("path integration") and for updating hippocampal location-specific firing. The contributions of ambulatory, vestibular, and optic self-motion signals to CA1 unit activity and EEG were studied while rats either walked or drove a car between locations on a circular track (referred to as WALK and CAR, respectively) or experienced pseudomotion, in which the animal was stationary and the environment was rotated (WORLD). Fewer pyramidal cells expressed place fields during CAR and those that did exhibited substantially larger place fields. The number of theta cycles required to traverse a place field increased, whereas the slope of the theta phase of firing versus position function was reduced. The presence and/or location of place fields were not well correlated between conditions. These effects were even more accentuated during WORLD. These results are not explainable by a simple "smearing out" of place fields but, in terms of size of place fields relative to the track size, are comparable with what would be observed if the track circumference was reduced and the animal moved around it at a correspondingly slower speed. Theta (and its 14 -18 Hz harmonic) power were dependent on velocity, but the gain of this function was substantially reduced during CAR and WORLD, again as if the rat were moving more slowly. The spatial scale over which the hippocampal population vector is updated appears to be derived primarily from the gain of a self-motion velocity signal with approximately equal components derived from ambulation, vestibular, and optic-flow signals.