Spatial relational memory in 9-month-old macaque monkeys

Abstract

This experiment assesses spatial and nonspatial relational memory in freely moving 9-mo-old and adult (11-13-yr-old) macaque monkeys (Macaca mulatta). We tested the use of proximal landmarks, two different objects placed at the center of an open-field arena, as conditional cues allowing monkeys to predict the location of food rewards hidden in one of two sets of three distinct locations. Monkeys were tested in two different conditions: (1) when local visual cues marked the two sets of potentially baited locations, so that monkeys could use both local and spatial information to discriminate these locations from never-baited locations; and (2) when no local visual cues marked the two sets of potentially baited locations, so that monkeys had to rely on a spatial relational representation of the environment to discriminate these locations. No 9-mo-old or adult monkey associated the presence of the proximal landmarks, at the center of the arena, with the presence of food in one set of three distinct locations. All monkeys, however, discriminated the potentially baited locations in the presence of local visual cues, thus providing evidence of visual discrimination learning. More importantly, all 9-mo-old monkeys tested discriminated the potentially baited locations in absence of the local visual cues, thus exhibiting evidence of spatial relational learning. These findings indicate that spatial memory processes characterized by a relational representation of the environment are present as early as 9 mo of age in macaque monkeys.The existence of multiple memory systems subserved by different neural substrates is a widely accepted view of memory organization in the mammalian brain (Cohen and Eichenbaum 1993;Milner et al. 1998;Eichenbaum 2000). Declarative (relational) memory was originally defined as the type of memory sensitive to lesion of the medial temporal lobe (the hippocampus in particular), whereas nondeclarative memory encompasses a set of disparate memory processes that are not sensitive to medial temporal lobe damage (Cohen and Squire 1980;Squire 1992). In rodents, declarative memory has been intensively investigated with tasks that assess spatial relational abilities in freely moving individuals (Olton and Samuelson 1976;O'Keefe and Nadel 1978;Morris 1981;Barnes 1988;Lavenex and Schenk 1995Schenk et al. 1995;. These tasks are readily learned and can easily be adapted to the ecological and ethological characteristics of different species ) including humans (Overman et al. 1996), thus enabling the comparative evaluation of learning and memory processes (Banta Lavenex et al. 2001). Spatial learning tasks in which subjects can move about freely in a controlled environment, in contrast, have only rarely been used to study memory processes in monkeys (but see Rapp et al. 1997;Rehbein and Moss 2002;Ludvig et al. 2003;Ma et al. 2003;Hampton and Murray 2004).We have adapted an experimental design originally developed to assess spatial cognition in rodents Schenk 1995, 1997;) in order to study the emergence of memory p...

Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

“…Each day, three locations on either the inner array or the outer array were baited. The location of the food changed pseudo-randomly between the two arrays between days, but remained the same between trials within a daily session 7,13 . For each trial, monkeys entered and exited the arena from one of the four pseudo-randomly chosen entrances.…”

“…Within-group analyses were conducted with choice type as the repeated measures. Because monkeys might have unique strategies for finding the food locations 13 , we also analyzed the behavior of each individual monkey separately to detect evidence of learning. In this case, statistical analyses were performed within subjects, with choice type as a factor and daily sessions as the repeated measures.…”

“…Monkeys began pre-training and acclimation 18.6 ± 0.3 months after surgery (sham-operated: 18.9 ± 0.6 months; hippocampus-lesioned: 18.5 ± 0.4 months). During a pre-training phase that took place in temporary holding cages (61 cm  66 cm  81 cm), monkeys were first trained to displace a plastic cup to retrieve grapes that were hidden underneath it 7,13 . Following pre-training, monkeys received one 5-min acclimation session per day for 5 d, during which they were free to explore the open-field arena.…”

“…In the second, the spatial relational condition, all cups were the same neutral color, so that the monkeys had to rely on an allocentric representation of the environment to discriminate between the potentially baited and never-baited locations. Multiple goals and four pseudo-randomly chosen entrance points prevented the monkeys from relying on an egocentric strategy to identify food locations 7,13 .…”

Spatial relational learning and memory abilities do not differ between men and women in a real-world, open-field environment

“…Our task tests allocentric, spatial relational memory [4,5,24,25], that is, the memory for spatial locations defined in relation to distant environmental cues (i.e., in a frame of reference centered on the objects constituting the environment), and which is therefore independent from the subject's own location or orientation (i.e., not centered on the subject's body position or egocentrically). Importantly, allocentric spatial memory has been shown in rodents and non-human primates to be dependent on the integrity of the hippocampal formation [4,5,20,34,39].…”