Review
Reliability of cortical activity during natural stimulation

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Response reliability is complementary to more conventional measurements of response amplitudes, and can reveal phenomena that response amplitudes do not. Here we review studies that measured reliability of cortical activity within or between human subjects in response to naturalistic stimulation (e.g. free viewing of movies). Despite the seemingly uncontrolled nature of the task, some of these complex stimuli evoke highly reliable, selective and time-locked activity in many brain areas, including some regions that show little response modulation in most conventional experimental protocols. This activity provides an opportunity to address novel questions concerning natural vision, temporal scale of processing, memory and the neural basis of inter-group differences.

Section snippets

Reliability of neuronal responses

Neuronal responses hypothesized to be more reliable (reproducible) under naturalistic stimulus conditions than under conventional laboratory conditions using artificial stimuli. Mechler et al. [1] reported that the responses of neurons in the visual cortex were more reliable for moving edges (abundant in natural vision) than for drifting sinusoidal gratings (common only in psychophysical experiments). Yao et al. [2] measured neural responses to movies of natural scenes; response reliability

Response reliability and response selectivity

An initial demonstration of response reliability to natural stimuli measured human brain activity during free viewing of a segment from The Good, the Bad and the Ugly, a well-known film by Sergio Leone (1966) [4]. Activity in the early auditory cortex serves as an illustrative example of the results (Figure 1). The responses in the auditory cortex (A1+, see Glossary for abbreviations of anatomically and functionally defined brain areas) of each subject were similar during repeated presentations

Response reliability versus response amplitude

The reliability of cortical activity can reveal phenomena that response amplitudes do not. To demonstrate this, eye movements and brain activity were measured simultaneously while subjects viewed movies (without sound tracks) played forward and backward in time [5]. The eye movements were highly reliable across viewers and very similar across repeated presentations of the same movie for both the forward and backward presentations, verifying that the level of engagement was comparable across the

Hierarchy of temporal receptive windows in the human cortex

It is well established that neurons along the visual cortical pathways have increasingly larger spatial receptive fields [25]. This is a basic organizing principle of the visual system; neurons in high-level visual areas receive input from many other neurons, in early visual areas, that have smaller receptive fields, thereby accumulating information over space. Real-world events occur not only over extended regions of space, but also over extended periods of time. It was hypothesized that a

Response reliability, neuronal spiking and fMRI in the human auditory cortex

Naturalistic stimulation, because it evokes highly reliable responses, can be used to relate different research techniques. For example, inter- and intra-SC were used to compare electrophysiological responses recorded from two epilepsy patients with the fMRI responses obtained from eleven healthy subjects who watched the same segment of Leone's movie The Good, the Bad and the Ugly [26]. The firing rates of 53 single neurons in Heschl's gyrus (auditory cortex) were recorded with intracranial

Encoding of real-world events into memory

Movies are encoded into memory even when subjects are not explicitly instructed to do so, and can be retained in memory for many months [27]. This tendency was exploited to study the neural basis of episodic encoding of realistic events. Memory for the narrative content of a TV episode was assessed three weeks after subjects watched it in the scanner [6]. To increase the ecological validity of the study, participants were not informed of a pending memory questionnaire and were not asked to

Inter-group differences in brain activity across clinical groups

Calculating inter-SC with typical healthy subjects might be used as a benchmark for detecting abnormalities in brain function in various clinical groups. The idea is simple: brain activity in any given clinical group (e.g., schizophrenia, autism, depression, anxiety) is hypothesized to be manifest in dysfunctional responses that deviate from the normal range, in a manner that is unique to each disorder. By comparing the responses in each brain area within a given clinical group to a normal

Response reliability in the ‘default mode’/’intrinsic system’ of brain areas

The ‘default mode’ 29, 30, 31, 32 brain areas, also termed the ‘intrinsic system’ [10], exhibit decreases in activity during external stimulation relative to rest. There has been much speculation about the possible functions of the ‘default mode’ 30, 33, 34, 35. Previous studies reported that these brain areas responded not only with low response amplitudes (below baseline) but also unreliably during free viewing of movies, as compared to sensory-motor areas 4, 10. This response profile has led

Conclusion and limitations

This paper reviews a series of studies that exploited inter- and intra-subject correlation to characterize the reliability of cortical response time courses across individuals. These studies found that under natural viewing conditions a large portion of the cortex evinces reliable, and selective, responses that are shared across all viewers 4, 5, 6, 7, 8, 9, 10. In contrast to the shared responses, some brain responses were reliable across repeated presentations only within a particular

Acknowledgements

Supported by an International Human Frontier Science Program Organization long-term fellowship (U.H.); National Institutes of Health Grants R01-MH69880 and R21-DA024423 (D.J.H.) and grants from the Weizmann–New York University Demonstration Fund in Neuroscience, the Israel Science Foundation, the Benozyio Center and the Minerva Foundation (R.M.). Special thanks to Barbara Knappmeyer for contributing to the acquisition and analysis of the Hitchcock data, and to David Carmel for comments on an

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