Single Neurons in the Monkey Hippocampus and Learning of New Associations

Abstract

The medial temporal lobe is crucial for the ability to learn and retain new declarative memories. This form of memory includes the ability to quickly establish novel associations between unrelated items. To better understand the patterns of neural activity during associative memory formation, we recorded the activity of hippocampal neurons of macaque monkeys as they learned new associations. Hippocampal neurons signaled learning by changing their stimulus-selective response properties. This change in the pattern of selective neural activity occurred before, at the same time as, or after learning, which suggests that these neurons are involved in the initial formation of new associative memories.

Comparison of population activity in the dorsal premotor cortex and putamen during the learning of arbitrary visuomotor mappings

“…Similar changes occur in the hippocampus during the learning of arbitrary visuomotor mappings (Wirth et al, 2003), also called object-in-scene learning. A comparison of the precise relative timing of neuronal activity changes in these various regions remains limited by small, yet significant differences in the methodology used from study to study.…”

“…Learning phases were defined in a manner similar to that of Chen and Wise (1995a), taking into account the method for detecting the onset of learning devised by Wirth et al (2003). Their method is called a state-space filter, and it detects the trial on which the lower 95% confidence limit of averaged performance first exceeds chance levels, which in this case and in theirs, was 25% correct.…”

“…Their method is called a state-space filter, and it detects the trial on which the lower 95% confidence limit of averaged performance first exceeds chance levels, which in this case and in theirs, was 25% correct. We divided trials for novel mappings into three groups: (1), an early phase of learning that incorporated all trials up to (but not including) the learning-criterion trial of Wirth et al (2003); (2) a middle phase of learning comprising trials from (and including) the same learning-criterion until the attainment of asymptotic performance, as identified by the first occurrence of three consecutive correct responses; and (3), all trials after reaching the asymptote. The latter group included the last trial of the series of three consecutive correct responses that defined the attainment of asymptotic performance.…”

“…A comparison of the precise relative timing of neuronal activity changes in these various regions remains limited by small, yet significant differences in the methodology used from study to study. Nevertheless, relative to the learning criterion trial as defined by Wirth et al (2003), hippocampal cells change their activity several trials earlier than do cells in the putamen and PMd (S. Wirth, E. Buch, S. Wise, and W. Suzuki, unpublished data). It seems likely that, together, the caudate nucleus (Pasupathy and Miller, 2005) and the hippocampus (Wirth et al, 2003) contribute most to the earliest phases of learning, and that PMd and the putamen play a critical role in more permanent storage for later recall.…”

“…Antecedents can include visual and other sensory inputs, and consequents usually involve movements or the targets of movement. Changes in task-related neuronal activity during arbitrary visuomotor learning have been described for dorsal premotor cortex (PMd) (Mitz et al, 1991;Brasted and Wise, 2004), supplementary eye field (Chen and Wise, 1995a, b), frontal eye field (Chen and Wise, 1995b), prefrontal cortex (Asaad et al, 1998;Pasupathy and Miller, 2005), hippocampus (Cahusac et al, 1993;Wirth et al, 2003), striatum Jog et al, 1999;Brasted and Wise, 2004;Pasupathy and Miller, 2005) and globus pallidus (Inase et al, 2001). Neuropsychological studies point to the same neural network (Petrides, 1985;Halsband and Passingham, 1985;Rupniak and Gaffan, 1987;Gaffan and Harrison, 1988;Canavan et al, 1989;Eacott and Gaffan, 1992;Murray and Wise, 1996;Ridley and Baker, 1997;Wang et al, 2000;Bussey et al, 2001Bussey et al, , 2002Brasted et al, 2002Brasted et al, , 2003Barefoot et al, 2002Barefoot et al, , 2003Nixon et al, 2004), as does the neuroimaging literature (Deiber et al, 1991(Deiber et al, , 1997Paus et al, 1993;Toni and Passingham, 1999;Toni et al, 2001Toni et al, , 2002Eliassen et al, 2003).…”