Memory-Guided Attention: Independent Contributions of the Hippocampus and Striatum
Summary
Memory can strongly influence how attention is deployed in future encounters. Though memory dependent on the medial temporal lobes has been shown to drive attention, how other memory systems could concurrently and comparably enhance attention is less clear. Here, we demonstrate that both reinforcement learning and context memory facilitate attention in a visual search task. Using functional magnetic resonance imaging, we dissociate the mechanisms by which these memories guide attention: trial by trial, the hippocampus (not the striatum) predicted attention benefits from context memory, while the striatum (not the hippocampus) predicted facilitation from rewarded stimulus-response associations. Responses in these regions were also distinctly correlated with individual differences in each type of memory-guided attention. This study provides novel evidence for the role of the striatum in guiding attention, dissociable from hippocampus-dependent context memory.
Introduction
Attention can be profoundly influenced by memory. Even something as simple as having previously viewed a picture or an array of shapes can inform where visual attention will be directed, enhancing perceptual sensitivity (Chun and Jiang, 1998, Patai et al., 2012, Summerfield et al., 2006). While the influence of memory on attention is a relatively recent topic (Hutchinson and Turk-Browne, 2012, Rosen et al., 2015), there is compelling evidence that hippocampal memory can guide attention. The hippocampal memory system rapidly encodes episodic memories, which are flexible and rich in contextual detail (Burgess et al., 2002Burgess et al., 2002). Long-term memory for complex scenes engages the hippocampus and facilitates attention and eye movements to targets, even in the absence of explicit recall (Hannula and Ranganath, 2009, Summerfield et al., 2006). The contextual cueing effect demonstrates that memory for a repeated spatial configuration guides attention and improves performance in visual search (Chun and Jiang, 1998Chun and Jiang, 1998). These memories depend on medial temporal lobe (MTL) structures and have frequently been shown to involve the hippocampus (Chun and Phelps, 1999, Giesbrecht et al., 2013, Greene et al., 2007, Preston and Gabrieli, 2008).
Although these studies have demonstrated the critical role of hippocampal memory in guiding attention, memory is not a unitary process (Squire, 1992Squire, 1992). Different neural systems support encoding and retrieval of specific kinds of information (Henke, 2010Henke, 2010). Thus, the ability of memory for diverse cues to guide attention may depend on distinct memory systems. Unlike hippocampal memory, the striatum slowly acquires rigid associations between stimuli and responses (Bayley et al., 2005, Graybiel, 1998, Yin and Knowlton, 2006). In healthy individuals, hippocampal and striatal systems can concurrently acquire information (Foerde and Shohamy, 2011Foerde and Shohamy, 2011), and lesion studies in rats (Packard and McGaugh, 1996Packard and McGaugh, 1996) and human patients (Knowlton et al., 1996Knowlton et al., 1996) have dissociated these systems. However, the influence of striatal memory on attention has not been studied.
We hypothesize that people can learn and use multiple informative cues to guide attention. Furthermore, we hypothesize that changing the type of cue can change the memory system that guides attention. We developed a way to directly compare how hippocampal and striatal memory influences attention. Contextual cueing demonstrates the impact of hippocampal memory on attention in visual search. During the search task, participants search for a target (a rotated “T”) and press a button once they find it, indicating the direction of the “T” (Figure 1Figure 1). The influence of hippocampal memory is shown via repeated configurations of target and distractors; on these trials, memory for spatial context guides attention to the exact location of the target. This effect is implicit. Participants do not have explicit memory for the repeated context (Chun and Jiang, 1998, Chun and Jiang, 2003, Chun and Phelps, 1999).
Experiment Design and Behavior
(A) Trial sequence.
(B) Example search screen and correct response.
(C) Schematic of CC and SR associations.
(D) Behavioral results. Participants were significantly faster at finding the “T” in the presence of a CC or SR cue compared to no cue (replication, Figure S1Figure S1). Left: learning throughout the experiment (one run = mean of four sequential blocks). Only responses for accurate, non-outlier trials are shown. Outliers were defined as RTs more than 3 SDs outside the mean for that trial type (1.5% of trials, no significant difference between trial types; Chun and Jiang, 2003Chun and Jiang, 2003). Right: performance during the second half of the experiment (gray background). Error bars, ±1 SE. ∗∗∗p < 0.001.
While contextual cueing has been frequently replicated and provides an index of hippocampal memory guiding attention, other forms of predictive associations, potentially reliant on other memory systems, have been less studied. To address this, we modified the search task to include probabilistic stimulus-response (SR) associations known to rely on the striatum as mnemonic cues for attention. Specifically, on some trials, the target and distractors appeared in a different color. The predictive color probabilistically (80% validity) cued the target location (quadrant of the screen) and the button-press response (the direction of the “T”). Thus, the cue evoked a “chunked” response of orienting to the quadrant and preparing the button press. The striatum is critical to forming such SR associations, including the chunking of motor and cognitive actions following a cue (e.g., Graybiel, 1998Graybiel, 1998). We randomly interleaved these cued trials, hereafter contextually cued (CC) and SR, with trials that had no mnemonic cue. The influence of both cues on attention was quantified as faster reaction time (RT) on cued compared to uncued trials.
Although these studies have demonstrated the critical role of hippocampal memory in guiding attention, memory is not a unitary process (Squire, 1992Squire, 1992). Different neural systems support encoding and retrieval of specific kinds of information (Henke, 2010Henke, 2010). Thus, the ability of memory for diverse cues to guide attention may depend on distinct memory systems. Unlike hippocampal memory, the striatum slowly acquires rigid associations between stimuli and responses (Bayley et al., 2005, Graybiel, 1998, Yin and Knowlton, 2006). In healthy individuals, hippocampal and striatal systems can concurrently acquire information (Foerde and Shohamy, 2011Foerde and Shohamy, 2011), and lesion studies in rats (Packard and McGaugh, 1996Packard and McGaugh, 1996) and human patients (Knowlton et al., 1996Knowlton et al., 1996) have dissociated these systems. However, the influence of striatal memory on attention has not been studied.
We hypothesize that people can learn and use multiple informative cues to guide attention. Furthermore, we hypothesize that changing the type of cue can change the memory system that guides attention. We developed a way to directly compare how hippocampal and striatal memory influences attention. Contextual cueing demonstrates the impact of hippocampal memory on attention in visual search. During the search task, participants search for a target (a rotated “T”) and press a button once they find it, indicating the direction of the “T” (Figure 1Figure 1). The influence of hippocampal memory is shown via repeated configurations of target and distractors; on these trials, memory for spatial context guides attention to the exact location of the target. This effect is implicit. Participants do not have explicit memory for the repeated context (Chun and Jiang, 1998, Chun and Jiang, 2003, Chun and Phelps, 1999).
Experiment Design and Behavior
(A) Trial sequence.
(B) Example search screen and correct response.
(C) Schematic of CC and SR associations.
(D) Behavioral results. Participants were significantly faster at finding the “T” in the presence of a CC or SR cue compared to no cue (replication, Figure S1Figure S1). Left: learning throughout the experiment (one run = mean of four sequential blocks). Only responses for accurate, non-outlier trials are shown. Outliers were defined as RTs more than 3 SDs outside the mean for that trial type (1.5% of trials, no significant difference between trial types; Chun and Jiang, 2003Chun and Jiang, 2003). Right: performance during the second half of the experiment (gray background). Error bars, ±1 SE. ∗∗∗p < 0.001.
Download (.96 MB ) While contextual cueing has been frequently replicated and provides an index of hippocampal memory guiding attention, other forms of predictive associations, potentially reliant on other memory systems, have been less studied. To address this, we modified the search task to include probabilistic stimulus-response (SR) associations known to rely on the striatum as mnemonic cues for attention. Specifically, on some trials, the target and distractors appeared in a different color. The predictive color probabilistically (80% validity) cued the target location (quadrant of the screen) and the button-press response (the direction of the “T”). Thus, the cue evoked a “chunked” response of orienting to the quadrant and preparing the button press. The striatum is critical to forming such SR associations, including the chunking of motor and cognitive actions following a cue (e.g., Graybiel, 1998Graybiel, 1998). We randomly interleaved these cued trials, hereafter contextually cued (CC) and SR, with trials that had no mnemonic cue. The influence of both cues on attention was quantified as faster reaction time (RT) on cued compared to uncued trials.
