Title: Single-neuron correlates of visual object representation in the human brain: effects of attention, memory, and choice
Abstract: Neurons in the medial temporal lobe (amygdala and hippocampus) are known to respond selectively to specific object categories, such as faces. This dissertation investigates two novel extensions of this work: (1) how are such neuronal responses influenced by where we attend; (2) how is category information used by the brain to make decisions.
The first question evaluated the representation of faces in the primate amygdala during naturalistic conditions, by recording from both human and macaque amygdala neurons during free viewing of arrays of images with concurrent eye tracking. We found that category-selective responses were very strongly modulated by where people, or monkeys, fixated (overt attention). Subsequent experiments in humans only further demonstrated that this effect holds even when people allocate visual attention while keeping central fixation (covert attention). In both monkeys and humans, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons. Response latencies were also notably shorter in monkeys than in humans.
To answer the second question, we investigated how visual representations in the medial temporal lobe are subsequently used to make two types of decisions: a recognition memory choice ("have you seen this image before?"), and a stimulus categorization choice ("Is this a face?"). We show that (i) there are distinct populations of cells in the medial frontal cortex (including anterior cingulate cortex, and supplementary motor cortex) encoding recognition memory or categorization-based choices; (ii) category-selective cells in the medial temporal lobe are insensitive to such task conditions; and (iii) spike-field coherence between field potentials in the medial temporal lobe and action potentials in the medial frontal cortex is enhanced during recognition memory choices. This suggests that inter-areal communication between these two brain regions may be facilitated selectively in tasks that rely on recognition memory-based information.
Taken together these two components of this dissertation provide novel insights into how visual object representations in the human brain are gated by attention, and how they are used in decisions. This work thus for the first time provides a comprehensive characterization of how single neurons in the human brain participate in the cycle from perception to action.