Date of Degree
PhD (Doctor of Philosophy)
Detecting and interpreting sensory events, and remembering those events in in the service of future actions, forms the foundation of all behavior. Each of these pillars of the so-called "perception-action cycle" have been topics of extensive inquiry throughout recorded history, with philosophical foundations provided by early BCE and CE periods (especially during the Classic and Renaissance eras) leading to intensive empirical study in the twentieth and twenty-first centuries. Such experiments have described detailed (but incomplete) behavioral functions reflecting perception and memory, and have begun to unravel the extraordinarily complex substrates of these functions in the nervous system. The current dissertation was motivated by these findings, with the goal of meaningfully extending our understanding of such processes through a multi-experiment approach spanning the behavioral and neurophysiological levels. The focus of these experiments is on short-term memory (STM), though as we shall see, STM is ultimately inseparable from sensory perception and is directly or indirectly associated with guidance of motor responses. It thus provides a nexus between the sensory inputs and motor outputs that describe interactions between the organism and environment.
In Chapter 2, previous findings from nonhuman primate literature describing relatively poor performance for auditory compared to visual or tactile STM inspired similar comparisons among modalities in humans. In both STM and recognition memory paradigms, accuracy is shown to be lowest for the auditory modality, suggesting commonalities among primate species. Chapters 3-5 examined STM processing in nonhuman primates at the behavioral and neurophysiological levels. In Chapter 3, a systematic investigation of memory errors produced by recycling memoranda across trials (proactive interference) is provided for the understudied auditory modality in monkeys. Such errors were ameliorated (but not completely eliminated) by increasing the proportions of unique memoranda presented within a session, and by separating successive trials by greater time intervals. In Chapter 4, previous results revealing a human memory advantage for audiovisual events (compared to unimodal auditory or visual events) inspired a similar comparison in monkeys using a concurrent auditory, visual, and audiovisual STM task. Here, the primary results conformed to a priori expectations, with superior performance observed on audiovisual trials compared to either unimodal trial type. Surprisingly, two of three subjects exhibited superior unimodal performance on auditory trials. This result contrasts with previous results in nonhuman primates, but can be interpreted in light of these subjects' extensive prior experience with unimodal auditory STM tasks. In Chapter 5, the same subjects performed the concurrent audiovisual STM task while activity of single cells and local cell populations was recorded within prefrontal cortex (PFC), a region known to exhibit multisensory integrative and memory functions. The results indicate that both of these functions converge within PFC, down to the level of individual cells, as evidenced by audiovisual integrative responses within mnemonic processes such as delay-related changes in activity and detection of repeated versus different sensory cues. Further, a disproportionate number of the recorded units exhibited such mnemonic processes on audiovisual trials, a finding that corresponds to the superior behavioral performance on these trials. Taken together, these findings reinforce the important role of PFC in STM and multisensory integration. They further strengthen the evidence that "memory" is not a unitary phenomenon, but can be seen as the outcome of processing within and among multiple subsystems, with substantial areas of overlap and separation across modalities. Finally, cross-species comparisons reveal substantial similarities in memory processing between humans and nonhuman primates, suggesting shared evolutionary heritage of systems underlying the perception-action cycle.
Evolution has endowed us with the remarkable ability to “remember” or store information that is not directly available to our senses. Though we may take it for granted, memory is fundamental to our daily lives, and more broadly, enables adaptive behavior and survival throughout the animal kingdom.
Given its general relevance to the human condition – and the debilitating conditions associated with memory loss – scientists have ambitiously pursued a detailed understanding of its functional properties and underlying biological mechanisms. Progress made largely within the past century has revealed memory as an extraordinarily complex phenomenon, orchestrated by networks of interacting brain regions, each comprising vast populations of individual cells with specialized functional roles.
Impressive though these discoveries may be, they amount to having assembled several thousand pieces of a billion-piece puzzle. The current work was inspired by these existing fragments, and brings several new pieces to the table.
One of the consistent findings in the current studies is that our ability to store information is dependent upon sensory modality. Thus, memory appears to be better for images than sounds, and even better for images and sounds presented together than for either alone. Physiological recordings within the frontal lobe revealed individual cells and local cell populations specialized for integrating such crossmodal information in memory, as well as other functions such as linking sensory events and behavioral choices separated by time. It is hoped that these findings will contribute to a more comprehensive portrait of memory against which pathologies can be meaningfully interpreted.
publicabstract, audiovisual integration, monkey, prefrontal cortex, proactive interference, rhesus macaque, single-unit recording
Copyright 2015 James Bigelow