title: Quantifying learning-dependent changes in the brain: Single-trial multivoxel pattern analysis requires slow event-related fMRI.
abstract: Single-trial analysis is particularly useful for assessing cognitive processes that are intrinsically dynamic, such as learning. Studying these processes with fMRI is problematic, as the low signal-to-noise ratio of fMRI requires the averaging over multiple trials, obscuring trial-by-trial changes in neural activation. The superior sensitivity of multivoxel pattern analysis over univariate analyses has opened up new possibilities for single-trial analysis, but this may require different fMRI designs. Here, we measured fMRI and pupil dilation responses during discriminant aversive conditioning, to assess associative learning in a trial-by-trial manner. The impact of design choices was examined by varying trial spacing and trial order in a series of five experiments (total n = 66), while keeping stimulus duration constant (4.5 s). Our outcome measure was the change in similarity between neural response patterns related to two consecutive presentations of the same stimulus (within-stimulus) and between patterns related to pairs of different stimuli (between-stimulus) that shared a specific outcome (electric stimulation vs. no consequence). This trial-by-trial similarity analysis revealed clear single-trial learning curves in conditions with intermediate (8.1-12.6 s) and long (16.5-18.4 s) intervals, with effects being strongest in designs with long intervals and counterbalanced stimulus presentation. No learning curves were observed in designs with shorter intervals (1.6-6.1 s), indicating that rapid event-related designs-at present, the most common designs in fMRI research-are not suited for single-trial pattern analysis. These findings emphasize the importance of deciding on the type of analysis prior to data collection.
authors.affiliation: Department of Clinical Psychology, University of Amsterdam, Amsterdam, The Netherlands.|Amsterdam Brain and Cognition (ABC), Amsterdam, The Netherlands.|Medical Research Council-Cognition and Brain Sciences Unit, Cambridge, UK.
authors.forename: Renée M
authors.initials: RM
authors.lastname: Visser
authors.affiliation: Amsterdam Brain and Cognition (ABC), Amsterdam, The Netherlands.|Department of Psychiatry, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Michelle I C
authors.initials: MI
authors.lastname: de Haan
authors.affiliation: Spinoza Centre for Neuroimaging, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Tinka
authors.initials: T
authors.lastname: Beemsterboer
authors.affiliation: Spinoza Centre for Neuroimaging, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Pia
authors.initials: P
authors.lastname: Haver
authors.affiliation: Department of Clinical Psychology, University of Amsterdam, Amsterdam, The Netherlands.|Amsterdam Brain and Cognition (ABC), Amsterdam, The Netherlands.
authors.forename: Merel
authors.initials: M
authors.lastname: Kindt
authors.affiliation: Amsterdam Brain and Cognition (ABC), Amsterdam, The Netherlands.|Spinoza Centre for Neuroimaging, University of Amsterdam, Amsterdam, The Netherlands.|Department of Brain and Cognition, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: H Steven
authors.initials: HS
authors.lastname: Scholte
mesh_terms: D000328:Adult; D001245:Association Learning / Q000502:physiology*; D001921:Brain / Q000502:physiology*; D001931:Brain Mapping / Q000379:methods*; D003214:Conditioning, Classical / Q000502:physiology; D004597:Electroshock; D005239:Fear / Q000502:physiology; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted / Q000379:methods; D059032:Learning Curve; D008279:Magnetic Resonance Imaging / Q000379:methods*; D008297:Male; D011680:Pupil / Q000502:physiology; D012815:Signal Processing, Computer-Assisted; D055815:Young Adult
keywords: Associative learning; Aversive conditioning; Multivoxel pattern analysis; Representational similarity analysis; Single-trial fMRI