S1 – Mechanisms of adaptation in different visual cortical areas: electrophysiology, functional imaging and computational modeling.

Friday, May 6, 12:00 – 2:00 pm, Royal Ballroom 1-3

Organizer: Rufin Vogels, Department Neuroscience, K.U. Leuven Medical School, Leuven, Belgium

Presenters: Adam Kohn, Department of Neuroscience, Albert Einstein College of Medicine, New York; Rufin Vogels, Department Neuroscience, K.U. Leuven Medical School, Leuven, Belgium; Kalanit Grill-Spector, Department of Psychology & Neurosciences Institute, Stanford University; Stephen J. Gotts, Laboratory of Brain and Cognition, NIMH/NIH, Bethesda

Symposium Description

Neural responses in many visual areas are usually reduced when repeating a visual stimulus. This adaptation or repetition suppression effect has recently aroused considerable interest because of the use of fMRI-adaptation to infer stimulus selectivities or invariances of neuronal populations in humans. The use of fMRI-adaptation necessitates an understanding of the mechanisms of adaptation. Given the increased use of fMRI-adaptation, we believe it is time to review our current understanding of the mechanisms of adaptation and their implications for the interpretation of functional imaging adaptation data. In the proposed symposium we will discuss experiments and computational work that provided new insights into the neural mechanisms of adaptation. Importantly, we will compare adaptation mechanisms in different visual areas in non-human and human primates. In addition, we will address adaptation effects of different neural measures, i.e. spiking activity, local field potentials and fMRI, and integrate these experimental data with recent computational work. We will have 4 speakers, giving each 30-minute talks (including 5 minutes of discussion time). Adam Kohn (Albert Einstein College of Medicine) will present his recent work on adaptation mechanisms in macaque primary visual cortex using microelectrode array recordings of populations of single neurons. These new data on orientation tuning and contrast sensitivity demonstrate a rich variety of adaptation effects which can be explained by a simple computational model, reconciling previous findings of effects of adaptation on tuning in areas V1 and MT. The second speaker, Rufin Vogels (K.U. Leuven), will review the effects of adaptation on the shape tuning of macaque inferior temporal cortex. He will compare adaptation effects of spiking activity and local field potentials (LFPs) and test predictions of different models of adaptation. The spiking activity and LFPs adaptation data agreed with input-dependent, but not response-dependent neural fatigue models. Kalanit Grill-Spector (Stanford University) will examine different models of adaptation using high-resolution fMRI in human ventral temporal cortex. She will compare adaptation effects in different ventral regions and across different adaptation paradigms in relation to predictions from different neural models of adaptation. These fMRI data suggest that different adaptation mechanisms underlie fMRI-adaptation in different brain regions and may differ between paradigms. The fourth speaker, Stephen Gotts (NIMH), will review computational work on adaptation mechanisms and relate these to physiological work in the macaque and human MEG and intracranial EEG recordings. This work suggests the need to consider synchronization of neural activity in addition to changes in the response level. It also links the behavioral improvement in performance with repetition to neural adaptation mechanisms.

The multi-region and multi-technique approach makes the proposed symposium rather unique and original. The symposium is of obvious interest to visual neuroscientists -students and faculty – and given the link between neural adaptation and perceptual aftereffects and repetition priming, this topic will also be of interest to visual psychophysicists. The attendees will gain insights into mechanisms of adaptation, which are crucial for interpreting fMRI-adaptation results and linking these with behavioral effects of stimulus repetition.

Presentations

The influence of surround suppression on adaptation effects in primary visual cortex

Adam Kohn, Department of Neuroscience, Albert Einstein College of Medicine, New York

Adaptation has been used extensively to probe mechanisms of visual processing. Neurophysiological studies have measured how adaptation affects single neurons, using stimuli tailored to evoke robust responses.

Understanding the consequences of adaptation, however, requires measuring effects on neural populations, which include many cells that are weakly driven by the adapter. To provide a more complete view of how adaptation affects neural responses, we implanted microelectrode arrays in primary visual cortex of macaque monkeys and measured orientation tuning and contrast sensitivity before and after prolonged adaptation with a range of stimuli. Whereas previous studies have emphasized that adaptation suppresses responsiveness and repels tuning (termed, stimulus-specific suppression), we find that adaptation can also lead to response facilitation and attractive shifts in V1 tuning. Using a simple computational model, we show that which of these effects occurs depends on the relative drive provided by the adapter to the receptive field and suppressive surround. Our data reveal a richer repertoire of adaptation effects than previously considered and provide a simple explanation for previously disparate findings concerning the effects of adaptation on tuning in V1 and MT. More generally, our results suggest an intimate relationship between spatial and temporal contextual effects, with implications for interpreting fMRI data and for understanding the functional role of rapid sensory-driven plasticity.

Mechanisms of adaptation of spiking activity and local field potentials in macaque inferior temporal cortex

Rufin Vogels, Department Neuroscience, K.U. Leuven Medical School, Leuven, Belgium

Several neural models have been proposed to explain adaptation effects in visual areas. We compared predictions derived from these models with adaptation effects of spiking activity and Local Field Potentials (LFPs) in macaque inferior temporal (IT) cortex. First, we compared the effect of brief adaptation on shape tuning using parameterized shape sets with predictions derived from fatigue and sharpening models. We found adaptation of spiking activity and of LFP power in the high-gamma (60-100 Hz) band. Contrary to sharpening but in agreement with fatigue models, repetition did not affect shape selectivity. The degree of similarity between adapter and test shape was a stronger determinant of adaptation than was the response to the adapter. The spiking and LFP adaptation effects agreed with input-, but not response-fatigue models. Second, we examined whether stimulus repetition probability affects adaptation, as predicted from the top-down, perceptual expectation model of Summerfield et al. (Nat. Neurosci., 2008). Monkeys were exposed to 2 interleaved trials, each consisting of 2 either identical (rep trial) or different stimuli (alt trial). Repetition blocks consisted of 75% (25%) of rep (alt) trials and alternation blocks had the opposite repetition probabilities. For both spiking and LFP activities, adaptation did not differ between these blocks. This absence of any repetition probability effect on adaptation suggests that adaptation in IT is not caused by contextual factors related to perceptual expectation, but instead agrees with bottom-up, fatigue-like mechanisms. We will discuss the implications of these single unit and LFP data for the interpretation of fMRI-adaptation studies.

fMRI-Adaptation in Human Ventral Temporal Cortex: Regional Differences Across Time Scales

Kalanit Grill-Spector, Dept. of Psychology & Neurosciences Institute, Stanford University

One of the most robust experience-related cortical dynamics is reduced neural activity when stimuli are repeated. This reduction has been linked to performance improvements due to repetition and also used to probe functional characteristics of neural populations. However, the underlying neural mechanisms are as yet unknown. Here, we consider two models that have been proposed to account for repetition-related reductions in neural activity, and evaluate them in terms of their ability to account for the main properties of this phenomenon as measured with fMRI (referred to as fMRI-adaptation, fMRI-A). I will describe results of recent experiments in which we investigated the effects of short-lagged (SL, immediate) and long-lagged (LL, many intervening stimuli) repetitions on category selectivity in human ventral temporal cortex (VTC) using high-resolution fMRI. We asked whether repetition produces scaling or sharpening of fMRI responses across VTC. Results illustrate that repetition effects across time scales vary qualitatively along a lateral-medial axis. In lateral VTC, both SL and LL repetitions produce scaling of fMRI responses. In contrast, medial VTC exhibits scaling effects during SL repetitions, but sharpening effects for LL repetitions. Finally, computer simulations linking neural repetition effects to fMRI-A show that different neural mechanisms likely underlie fMRI-A in medial compared to lateral VTC. These results have important implications for future fMRI-A experiments because they suggest that fMRI-A does not reflect a universal neural mechanism and that results of fMRI-A experiments will likely be paradigm independent in lateral VTC, but paradigm dependent in medial VTC.

Mechanisms of repetition suppression in models, monkeys, and humans: A case for greater efficiency through enhanced synchronization

Stephen J. Gotts, Laboratory of Brain and Cognition, NIMH/NIH, Bethesda

Experience with visual objects leads to later improvements in identification speed and accuracy (”repetition priming”), but generally leads to reductions in neural activity in single-cell recording studies in monkeys and fMRI studies in humans (”repetition suppression”). While the cell mechanisms that lead to these activity reductions are unclear, previous studies have implicated relatively local, automatic cortical mechanisms, and slice physiological recordings have identified several candidate short- and long-term plasticity mechanisms. I will show that these plasticity mechanisms when incorporated into a simplified neocortical circuit model are capable of re-producing changes in stimulus selectivity due to repetition as seen in single-cell recording studies in monkey area TE: ”scaling” with relatively short-term repetitions and ”sharpening” over longer periods of experience. However, these simulations when based on average firing rate fail to provide an account of behavioral priming. In contrast, simulations that retain the spiking property of neurons can potentially account for both repetition suppression and priming by allowing more synchronized and temporally coordinated activity at lower overall rates. I will review the current state of evidence in support of this proposal from monkey single-cell and LFP recordings and human MEG. I will also present new data from intracranial EEG recordings of human epilepsy patients showing that stimulus repetition at both short and long time scales leads to larger amplitude activity fluctuations at low frequencies (< 15 Hz). These results indicate that greater neural synchronization accompanies lower overall activity levels following stimulus repetition, constituting a novel efficiency mechanism.