Fast Learning of Simple Perceptual Discriminations Reduces Brain Activation in Working Memory and in High-Level Auditory Regions
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Fast Learning of Simple Perceptual Discriminations Reduces Brain Activation in Working Memory and in High-level Auditory Regions Luba Daikhin and Merav Ahissar Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/27/7/1308/1783003/jocn_a_00786.pdf by MIT Libraries user on 17 May 2021 Abstract ■ Introducing simple stimulus regularities facilitates learning tion induced a larger activation in frontoparietal areas known to of both simple and complex tasks. This facilitation may reflect be part of the working memory network. However, only the an implicit change in the strategies used to solve the task when condition with a reference showed fast learning, which was successful predictions regarding incoming stimuli can be accompanied by a reduction of activity in two regions: the left formed. We studied the modifications in brain activity associa- intraparietal area, involved in stimulus retention, and the pos- ted with fast perceptual learning based on regularity detection. terior superior-temporal area, involved in representing auditory We administered a two-tone frequency discrimination task and regularities. We propose that this joint reduction reflects a re- measured brain activation (fMRI) under two conditions: with duction in the need for online storage of the compared tones. and without a repeated reference tone. Although participants We further suggest that this change reflects an implicit strategic could not explicitly tell the difference between these two con- shift “backwards” from reliance mainly on working memory net- ditions, the introduced regularity affected both performance works in the “No-Reference” condition to increased reliance on and the pattern of brain activation. The “No-Reference” condi- detected regularities stored in high-level auditory networks. ■ INTRODUCTION rarely been studied, although it is probably crucial to The dynamics of perceptual learning, particularly its ini- subsequent learning dynamics (e.g., Ortiz & Wright, tial stages, are not well understood. Previous studies have 2009; Hawkey, Amitay, & Moore, 2004; Karni, Jezzard, focused on the specificity of learning to trained stimuli, Adams, Turner, & Ungerleider, 1995). which was shown to be consistent with the specificity One of the key features of the training procedure, par- of the sensory areas (Spang, Grimsen, Herzog, & Fahle, ticularly at the early training stages, is the consistency of 2010; Van Wassenhove & Nagarajan, 2007; Amitay, Hawkey, stimuli across consecutive trials. Consistent training with & Moore, 2005; Seitz & Watanabe, 2005; Demany & similar stimuli leads to fast, condition-specific (Cohen, Semal, 2002; Ahissar & Hochstein, 1993, 1996; Levi & Daikhin, & Ahissar, 2013) learning (e.g., Otto, Herzog, Polat, 1996; Karni & Sagi, 1991). However, such speci- Fahle, & Zhaoping, 2006), whereas training with a broad ficity mainly characterizes later stages of learning, when range of stimuli, whose sequence is not predictable, leads some expertise had been obtained (Jeter, Dosher, Liu, & to slow learning (Parkosadze, Otto, Malaniya, Kezeli, & Lu, 2010; Ahissar & Hochstein, 1997; Karni & Sagi, Herzog, 2008) if any (e.g., Kuai, Zhang, Klein, Levi, & 1993). Ahissar and Hochstein (Ahissar, Nahum, Nelken, Yu, 2005; Adini, Wilkonsky, Haspel, Tsodyks, & Sagi, & Hochstein, 2009; Ahissar & Hochstein, 1997, 2004) 2004; Yu, Klein, & Levi, 2004). A very clear example of suggested that when finer resolution is required, per- this dissociation was recently reported in the auditory ceptual learning may progress backwards along the per- modality for training on frequency (pitch) discrimination ceptual hierarchy from crude generalizing representations between sequentially presented tones. Whereas dis- to more local ones. This theory, termed the Reverse crimination between tones whose frequency was ran- Hierarchy Theory, posits that perceptual learning is not domly chosen from a broad frequency range improved limited to a specific brain site and progresses from high- slowly (within hundreds of trials), substantial and fast to lower-level areas with practice. Nevertheless, it does improvement was achieved when the first tone in a pair not address the brain mechanisms underlying the very had a fixed frequency (Nahum, Daikhin, Lubin, Cohen, & early stages of learning, when the task and its broad Ahissar, 2010). This rapid improvement was attributed to stimulus characteristics need to be sorted out. This initial the ability to form effective predictions for the incoming stage is typically short and difficult to track and hence has stimuli when training with stimuli that obeyed a simple regularity (Ahissar et al., 2009; Ahissar & Hochstein, 2004). Here we inquired whether the impact of intro- The Hebrew University of Jerusalem ducing simple regularities that facilitate learning, perhaps © 2015 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 27:7, pp. 1308–1321 doi:10.1162/jocn_a_00786 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00786 by guest on 28 September 2021 by facilitating the “reverse hierarchy” process, is accom- initial stages of learning the regularity and then decrease panied by a detectable concurrent change in the pattern its activity with repetitions of this regularity (Karni et al., of brain activation. 1995, 1998), as long as the reference containing condi- Although serial discrimination is considered a simple tion is not interrupted. perceptual task, it requires two types of management To test these hypotheses, we measured both behavior processes, both of which involve frontoparietal networks. and the BOLD response when participants performed a First, as in any new task (or situation), its basic structure simple perceptual two-tone frequency discrimination in terms of neural representations should be set (Miller task. On the basis of the observations of Nahum, Daikhin, Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/27/7/1308/1783003/jocn_a_00786.pdf by MIT Libraries user on 17 May 2021 & Cohen 2001). Many studies suggest that this task- et al. (2010), participants in the current study were setting is implemented by high-level networks, which administered the following two conditions. In one, the include extensive frontal and parietal regions. These same tone was consistently presented in the first interval networks are largely general-purpose and form the of each trial. This regularity is known to be detected “task-set” for various tasks (and were hence termed “the quickly and yields fast and substantial improvement multiple-demand” network; Duncan, 2010; Duncan & (Cohen et al., 2013; Nahum, Daikhin, et al., 2010). In Owen, 2000). Second, task performance requires the the second condition, the same task and similar stimuli retention of the relevant value of the first stimulus in each (though drawn from a broader frequency range) were trial during the interstimulus interval and a comparison of used, but there was no cross-trial tone repetition. In this this value with that of the second stimulus. This retain- condition, participants’ improvement has been reported and-compare process is a working memory operation to be very slow and does not reach the same level of (e.g., Romo, Brody, Hernández, & Lemus, 1999). Such performance even after many practice sessions. operations were also shown to activate frontoparietal Wepresentedblocksofthesetwoconditionsinaninter- regions, which were thus termed the working memory leaved manner (3 blocks of one condition followed by network (Fedorenko, Behr, & Kanwisher, 2011; Koelsch 3 blocks of the other condition). Because the stimuli were et al., 2009; Baldo & Dronkers, 2006; Rainer, Asaad, & similar and the task was the same, participants were unaware Miller, 1998). The exact role of this network in the retain- of the switch in conditions. We asked which brain areas and-compare operation is still being debated. Previous were sensitive to the difference between the two conditions, studies have suggested that these working memory areas and activity in which brain areas was modified as a function both manage and store the task-relevant stimuli. However, of the rapid improvement we anticipated in the condition very recent studies (reviewed in Sreenivasan, Curtis, & involving a simple, easily detected stimulus regularity. D’Esposito, 2014) posit that the stimuli are stored in pos- terior sensory areas, and the role of the working memory network primarily involves task-related management. METHODS “ ” Additional related term is attentional resources, whose Participants recruitment when a task is generally more demanding also activate partially overalapping posterior-parietal regions Nineteen participants (age = 29 ± 5 years; 10 women) (Magen, Emmanouil, McMains, Kastner, & Treisman, 2009). took part in the study. Each of them performed fre- The behavioral observation that a simple regularity in quency discrimination and another task (not reported perceptual discriminations leads to fast perceptual learn- here) in the magnet (except one, who was administered ing, which is specific to the trained regularity (Cohen only the frequency discrimination task) and had an addi- et al., 2013; Nahum, Daikhin, et al., 2010), implies that tional anatomical scan at the end of the session. Before the load on management processes decreases. This de- entering the scanner, participants practiced a short version crease is expected because utilizing the regularity, that of the behavioral protocol that they performed during is, the repeated reference,