Experience‐dependent modifications of hippocampal place cell firing

Abstract

Understanding the empirical rules that regulate alterations of hippocampal firing fields will enhance our understanding of hippocampal function. The current study sought to extend previous research in this area by examining the effect of substituting a new stimulus for a familiar stimulus in a familiar environment. Hippocampal place cells were recorded while rats chased food pellets scattered onto the floor of a cylindrical apparatus with a white cue card affixed to the apparatus wall. Once a place cell had been recorded in the presence of the white card, the white card was replaced by a black card of the same size and shape. The place cell was then recorded in the presence of the black card. Thirty-six cells were recorded using this procedure. All cells had stable firing fields in the presence of the white card. Both the white and black cards had stimulus control over place cell firing; generally, rotation of either card caused an equal rotation of the firing fields present. When the black card was substituted for the white card, place cells showed time-variant changes in their spatial firing patterns. The change was such that the spatial firing patterns of the majority of place cells were similar in the presence of the white and black cards during initial black card exposures. During subsequent presentations of the black card, the spatial firing patterns associated with the 2 cards became distinct from each other. Once the differentiation of firing patterns had occurred in a given rat, all place cells subsequently recorded from that rat had different firing patterns in the presence of the white and black cards. The findings are discussed relative to sensory-, motor-, attentional-, and learning-related interpretations of hippocampal function. It is argued that the time-variant alteration of place cell firing fields observed following exposure to a novel stimulus in this study reflects an experience-dependent modification of place cell firing patterns.

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

“…Qualitatively, firing fields recorded in the presence of a 45° white card and a 45° black card separated by 135° appear the same as fields recorded with other card configurations (Muller and Kubie 1987; Sharp et al 1990; Bostock et al 1991; Hetherington and Shapiro 1997). In standard sessions, the average field size was 678 ± 502 cm 2 , so that the average field occupied 17% of the apparatus area.…”

“…Previous work showed that rotations of a single white card or a single black card caused equal rotations of firing fields (Muller and Kubie 1987; Bostock et al 1991). To establish that the card pair exerted similar strong stimulus control, we therefore ran at least one equal card rotation session for each rat.…”

“…We then asked how firing fields were affected if the angular distance between the two cards was made either smaller or greater by 25°. These “reconfigurations” did not cause fields to disappear nor to move over large distances as occurs in remapping (Muller and Kubie 1987; Thompson and Best 1989; Bostock et al 1991; Kentros et al 1998), allowing us to look for patterns of field movements across the cell sample.…”

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

“…First, O'Keefe and Burgess 1996 focused on the shape of the apparatus, to the exclusion of “marker” stimuli. Our two-card experiments are a new line of evidence that nonstructural aspects of the stimulus environment can be major determinants of firing field activity (see also Sharp et al 1990; Bostock et al 1991; Kentros et al 1998). This is not, however, a fundamental issue; the feature-based theory of O'Keefe and Burgess 1996 can be modified to include marker stimuli as well as walls.…”

“…In line with earlier work, we define similarity as the z transform of the pixel-by-pixel correlation coefficient ( r ) for a pair of positional firing rate patterns (Bostock et al 1991). To begin, one rate pattern is superimposed on the other and a paired list is made of the time-averaged firing rates in a pixel; a pixel is included in the list only if its rate was greater than zero in at least one session.…”