Note Inside out: A neuro-behavioral signature of free recall dynamics Irit Shapira-Lichter a,n , Eli Vakil c , Yifat Glikmann-Johnston a , Tali Siman-Tov a , Dan Caspi b,d , Daphna Paran b,d , Talma Hendler a,d,e Q1 a Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, 6 Weizmann Street, Tel Aviv 64239, Israel b Department of Rheumatology, Tel-Aviv Sourasky Medical Center, Israel c Department of Psychology and Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Israel d Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel e Department of Psychology, Tel-Aviv University, Tel-Aviv, Israel article info Article history: Received 21 September 2011 Received in revised form 20 May 2012 Accepted 25 May 2012 Keywords: Episodic memory Default mode network Hippocampus fMRI Inter-response times Memory search abstract Free recall (FR) is a ubiquitous internally-driven retrieval operation that crucially affects our day-to-day life. The neural correlates of FR, however, are not sufficiently understood, partly due to the methodological challenges presented by its emerging property and endogenic nature. Using fMRI and performance measures, the neuro-behavioral correlates of FR were studied in 33 healthy participants who repeatedly encoded and retrieved word-lists. Retrieval was determined either overtly via verbal output (Experiment 1) or covertly via motor responses (Experiment 2). Brain activation during FR was characterized by two types of performance-based parametric analyses of retrieval changes over time. First was the elongation in inter response time (IRT) assumed to represent the prolongation of memory search over time, as increased effort was needed. Using a derivative of this parameter in whole brain analysis revealed the default mode network (DMN): longer IRT within FR blocks correlated with less deactivation of the DMN, representing its greater recruitment. Second was the increased number of words retrieved in repeated encoding-recall cycles, assumed to represent the learning process. Using this parameter in whole brain analysis revealed increased deactivation in the DMN (i.e., less recruitment). Together our results demonstrate the naturally occurring dynamics in the recruitment of the DMN during utilization of internally generated processes during FR. The contrasting effects of increased and decreased recruitment of the DMN following dynamics in memory search and learning, respectively, supports the idea that with learning FR is less dependent on neural operations of internally-generated processes such as those initially needed for memory search. & 2012 Published by Elsevier Ltd. 1. Introduction Free recall (FR) is an internally guided retrieval operation, dependent on effective utilization of cognitive strategies with minimal support of external cues (Shimamura, 1995). Despite its profound effect on our daily routine and role in major mental declines (Nohara et al., 2000; Schmiedt, Meistrowitz, Schwendemann, Herrmann, & Basar-Eroglu, 2005; Zakzanis, 1998), to date only a limited number of studies have used in- vivo electrophysiological or neuroimaging techniques to study FR operations while most studies have focused on more externally driven modes of retrieval, such as recognition (Spaniol et al., 2009). One explanation for this research bias might be the endogenous nature of FR, which precludes animal studies and imposes a significant methodological challenge in a human brain imaging set-up. Another reason for this bias is that characteriza- tion of FR selectivity with respect to other retrieval operations such as cued recall or recognition is confounded by the inherent physical differences between them (e.g., silence in FR versus stimuli in cued recall or recognition). Several previous studies overcame these difficulties by com- paring different types of FR tasks/responses: correct and incorrect FR responses were compared in an intracranial EEG study (Sederberg et al., 2007), supra-span and sub-span FR periods were compared in a PET study (Grasby et al., 1993), and FR responses with and without semantic clustering were compared in an fMRI study (Long, Oztekin, & Badre, 2010). In another fMRI study, the brain activity patterns that preceded the retrieval of items belonging to different semantic categories were classified (Polyn, Natu, Cohen, & Norman, 2005). In the present study an alternative experimental approach was applied, namely, probing the neural signature of FR dynamics in time. To overcome the hurdles associated with the endogenous nature of FR, it was studied via behavioral manifestations of one of the central 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 71 73 75 77 79 81 83 85 87 89 Contents lists available at SciVerse ScienceDirect journal homepage: www.elsevier.com/locate/neuropsychologia Neuropsychologia 0028-3932/$ - see front matter & 2012 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.neuropsychologia.2012.05.028 n Corresponding author. Tel.: þ972 3 6974818; fax: þ972 2 6973080. E-mail address: iritlichter@yahoo.com (I. Shapira-Lichter). Please cite this article as: Shapira-Lichter, I., et al. Inside out: A neuro-behavioral signature of free recall dynamics. Neuropsychologia (2012), http://dx.doi.org/10.1016/j.neuropsychologia.2012.05.028 Neuropsychologia ] (]]]]) ]]]–]]]