Differential effects of experience on tuning properties of macaque MTL neurons in a passive viewing task

Abstract

The structures of the medial temporal lobe (MTL) have been shown to be causally involved in episodic and recognition memory. However, recent work in a number of species has demonstrated that impairments in recognition memory seen following lesions of the perirhinal cortex can be accounted for by deficits in perceptual discrimination. These findings suggest that object representation, rather than explicit recognition memory signals, may be crucial to the mnemonic process. Given the large amount of visual information encountered by primates, there must be a reconsideration of the mechanisms by which the brain efficiently stores visually presented information. Previous neurophysiological recordings from MTL structures in primates have largely focused on tasks that implicitly define object familiarity (i.e., novel vs. familiar) or contain significant mnemonic demands (e.g., conditional associations between two stimuli), limiting their utility in understanding the mechanisms underlying visual object recognition and information storage. To clarify how different regions in the MTL may contribute to visual recognition we recorded from three rhesus macaques performing a passive viewing task. The task design systematically varies the relative familiarity of different stimuli enabling an examination of how neural activity changes as a function of experience. The data collected during this passive viewing task revealed that neurons in the MTL are generally not sensitive to the relative familiarity of a stimulus. In addition, when the specificity (i.e., which images a neuron was selective for) of individual neurons was analyzed, there was a significant dissociation between different medial temporal regions, with only neurons in TF, but not CA3 or the perirhinal cortex, altering their activity as stimuli became familiar. The implications of these findings are discussed in the context of how MTL structures process information during a passive viewing paradigm.

Development of tube tetrodes and a multi-tetrode drive for deep structure electrophysiological recordings in the macaque brain

“…In the past, tetrodes have aided extensively in pursuing such research directions with primates, because of their advantages over conventional electrodes in the number and isolation quality of single units recorded (Gray et al, 1995;Tolias et al, 2007). However, mostly recently, but sparsely, TWTs have been used for recordings in deeper structures of the macaque brain (Erickson and Desimone, 1999;Erickson et al, 2000;Santos et al, 2012;Skaggs et al, 2007;Thome et al, 2012). The TuTes reported here are ideal for such a purpose, since, not only do they overcome any limitations of depth recordings with tetrodes, but also provide a solution with minimal amount of tissue damage along the electrode path.…”

“…While other groups have tried to address this need by building microdrives suited for driving tetrodes to multiple cortical and subcortical areas at the same time, the tissue damage resulting from the cannulae used has been a valid and ethical issue. Chronically implanted microdrives with tetrodes have also been utilized in the past for deep brain electrophysiology (Skaggs et al, 2007;Thome et al, 2012). A difficult parameter to judge is whether, the daily insertion of several smaller TuTes would cause less or more damage as compared to a one time implantation of a thicker guide tube enclosing a tetrode.…”

“…Further, splaying of the tetrode tips has been a valid concern during chronic implantation (Jog et al, 2002). Because of these constraints, their use for electrophysiological recordings in primates in deep structures has been relatively sparse and just recently reported (Erickson and Desimone, 1999;Erickson et al, 2000;Feingold et al, 2012;Santos et al, 2012;Skaggs et al, 2007;Thome et al, 2012). Among these, earlier studies employed tetrodes for electrical recording in the perirhinal cortex of the macaque using a telescoping guide tube system with twisted wire tetrodes glued inside 30 gauge stainless steel tubes (Erickson and Desimone, 1999;Erickson et al, 2000).…”

“…Among these, earlier studies employed tetrodes for electrical recording in the perirhinal cortex of the macaque using a telescoping guide tube system with twisted wire tetrodes glued inside 30 gauge stainless steel tubes (Erickson and Desimone, 1999;Erickson et al, 2000). More recently, they have been used within a chronically implanted 'hyperdrive', which permitted recordings at depths of 30-50 mm below the brain surface, in the hippocampus (Skaggs et al, 2007;Thome et al, 2012). However, the spatial position of these tetrodes in such a configuration is fixed at the time of implantation and can only be manipulated in depth, thus allowing only a limited area of the brain to be sampled.…”

“…A custom drive, for holding and advancing up to 5 tetrodes independently was also developed. These novel TuTes are in size about 10-20% of that of the cannulae, which have been used in the most recent studies (Erickson and Desimone, 1999;Erickson et al, 2000;Feingold et al, 2012;Santos et al, 2012;Skaggs et al, 2007;Thome et al, 2012).…”