Aidan J. Horner

Priming, response learning and repetition suppression.

Prior exposure to a stimulus can facilitate its subsequent identification and classification, a phenomenon called priming. This behavioural facilitation is usually accompanied by a reduction in neural response within specific cortical regions (repetition suppression, RS). Recent research has suggested that both behavioural priming and RS can be largely determined by previously learned stimulus–response associations. According to this view, a direct association forms between the stimulus presented and the response made to it. On a subsequent encounter with the stimulus, this association automatically cues the response, bypassing the various processing stages that were required to select that response during its first presentation. Here we reproduce behavioural evidence for such stimulus–response associations, and show the PFC to be sensitive to such changes. In contrast, RS within ventral temporal regions (such as the fusiform cortex), which are usually associated with perceptual processing, is shown to be robust to response changes. The present study therefore suggests a dissociation between RS within the PFC, which may be sensitive to retrieval of stimulus–response associations, and RS within posterior perceptual regions, which may reflect facilitation of perceptual processing independent of stimulus–response associations.

Stimulus-response bindings in priming

Highlights • S–R bindings are more flexible and pervasive than previously thought.• S–R bindings can simultaneously encode multiple stimulus and response representations.• S–R bindings can be encoded or retrieved in the absence of attention or awareness.• S–R bindings complicate interpretations of priming, but are interesting in their own right.• S–R bindings enable rapid yet context-dependent behaviors.

Bindings between Stimuli and Multiple Response Codes Dominate Long-Lag Repetition Priming in Speeded Classification Tasks.

Repetition priming is often thought to reflect the facilitation of 1 or more processes engaged during initial and subsequent presentations of a stimulus. Priming can also reflect the formation of direct, stimulus-response (S-R) bindings, retrieval of which bypasses many of the processes engaged during the initial presentation. Using long-lag repetition priming of semantic classification of visual stimuli, the authors used task switches between study and test phases to reveal several signatures of S-R learning in Experiments 1 through 5. Indeed, the authors found surprisingly little, if any, evidence of priming that could not be attributed to S-R learning, once they considered the possibility that stimuli are simultaneously bound to multiple, different response codes. Experiments 6 and 7 provided more direct evidence for independent contributions from at least 3 levels of response representation: the action (e.g., specific finger used), the decision (e.g., yes-no), and the task-specific classification (e.g., bigger-smaller). Although S-R learning has been discussed previously in many contexts, the present results go beyond existing theories of S-R learning. Moreover, its dominant role brings into question many interpretations of priming during speeded classification tasks in terms of perceptual-conceptual processing.

Synchronization of Medial Temporal Lobe and Prefrontal Rhythms in Human Decision Making

Optimal decision making requires that we integrate mnemonic information regarding previous decisions with value signals that entail likely rewards and punishments. The fact that memory and value signals appear to be coded by segregated brain regions, the hippocampus in the case of memory and sectors of prefrontal cortex in the case of value, raises the question as to how they are integrated during human decision making. Using magnetoencephalography to study healthy human participants, we show increased theta oscillations over frontal and temporal sensors during nonspatial decisions based on memories from previous trials. Using source reconstruction we found that the medial temporal lobe (MTL), in a location compatible with the anterior hippocampus, and the anterior cingulate cortex in the medial wall of the frontal lobe are the source of this increased theta power. Moreover, we observed a correlation between theta power in the MTL source and behavioral performance in decision making, supporting a role for MTL theta oscillations in decision-making performance. These MTL theta oscillations were synchronized with several prefrontal sources, including lateral superior frontal gyrus, dorsal anterior cingulate gyrus, and medial frontopolar cortex. There was no relationship between the strength of synchronization and the expected value of choices. Our results indicate a mnemonic guidance of human decision making, beyond anticipation of expected reward, is supported by hippocampal–prefrontal theta synchronization.

Stimulus–response bindings code both abstract and specific representations of stimuli: evidence from a classification priming design that reverses multiple levels of response representation

Repetition priming can be caused by the rapid retrieval of previously encoded stimulus–response (S–R) bindings. S–R bindings have recently been shown to simultaneously code multiple levels of response representation, from specific Motor-actions to more abstract Decisions (“yes”/”no”) and Classifications (e.g., “man-made”/”natural”). Using an experimental design that reverses responses at all of these levels, we assessed whether S–R bindings also code multiple levels of stimulus representation. Across two experiments, we found effects of response reversal on priming when switching between object pictures and object names, consistent with S–R bindings that code stimuli at an abstract level. Nonetheless, the size of this reversal effect was smaller for such across-format (e.g., word–picture) repetition than for within-format (e.g., picture–picture) repetition, suggesting additional coding of format-specific stimulus representations. We conclude that S–R bindings simultaneously represent both stimuli and responses at multiple levels of abstraction.

Grid-like Processing of Imagined Navigation

Summary Grid cells in the entorhinal cortex (EC) of rodents [1] and humans [2] fire in a hexagonally distributed spatially periodic manner. In concert with other spatial cells in the medial temporal lobe (MTL) [3, 4, 5, 6], they provide a representation of our location within an environment [7, 8] and are specifically thought to allow the represented location to be updated by self-motion [9]. Grid-like signals have been seen throughout the autobiographical memory system [10], suggesting a much more general role in memory [11, 12]. Grid cells may allow us to move our viewpoint in imagination [13], a useful function for goal-directed navigation and planning [12, 14, 15, 16], and episodic future thinking more generally [17, 18]. We used fMRI to provide evidence for similar grid-like signals in human entorhinal cortex during both virtual navigation and imagined navigation of the same paths. We show that this signal is present in periods of active navigation and imagination, with a similar orientation in both and with the specifically 6-fold rotational symmetry characteristic of grid cell firing. We therefore provide the first evidence suggesting that grid cells are utilized during movement of viewpoint within imagery, potentially underpinning our more general ability to mentally traverse possible routes in the service of planning and episodic future thinking.

A rapid, hippocampus-dependent, item-memory signal that initiates context memory in humans.

Summary The hippocampus, a structure located in the temporal lobes of the brain, is critical for the ability to recollect contextual details of past episodes. It is still debated whether the hippocampus also enables recognition memory for previously encountered context-free items. Brain imaging [1, 2] and neuropsychological patient studies [3, 4] have both individually provided conflicting answers to this question. We overcame the individual limitations of imaging and behavioral patient studies by combining them and observed a novel relationship between item memory and the hippocampus. We show that interindividual variability of hippocampal volumes in a large patient population with graded levels of hippocampal volume loss and controls correlates with context, but not item-memory performance. Nevertheless, concurrent measures of brain activity using magnetoencephalography reveal an early (350 ms) but sustained hippocampus-dependent signal that evolves from an item signal into a context memory signal. This is temporally distinct from an item-memory signal that is not hippocampus dependent. Thus, we provide evidence for a hippocampus-dependent item-memory process that initiates context retrieval without making a substantial contribution to item recognition performance. Our results reconcile contradictory evidence concerning hippocampal involvement in item memory and show that hippocampus-dependent mnemonic processes are more rapid than previously believed.

Replay of very early encoding representations during recollection

Long-term memories are linked to cortical representations of perceived events, but it is unclear which types of representations can later be recollected. Using magnetoencephalography-based decoding, we examined which brain activity patterns elicited during encoding are later replayed during recollection in the human brain. The results show that the recollection of images depicting faces and scenes is associated with a replay of neural representations that are formed at very early (180 ms) stages of encoding. This replay occurs quite rapidly, ∼500 ms after the onset of a cue that prompts recollection and correlates with source memory accuracy. Therefore, long-term memories are rapidly replayed during recollection and involve representations that were formed at very early stages of encoding. These findings indicate that very early representational information can be preserved in the memory engram and can be faithfully and rapidly reinstated during recollection. These novel insights into the nature of the memory engram provide constraints for mechanistic models of long-term memory function.

Categorical encoding of color in the brain

Significance Humans group the millions of discriminable colors into discrete categories, such as “blue” and “green.” There has been much debate about where color categories come from; for example, whether color categories are inbuilt into the visual system. We use functional MRI to identify regions of the brain that categorize color. Color categories are encoded by regions of the frontal lobes, which also categorize other information (e.g., sounds). Interestingly, the visual cortex responds only to the size of color differences, but not color categories. We conclude that color categories occur at the level of attention rather than being inbuilt into the visual system. The findings shed light on how the brain categorizes information and how it processes color. The areas of the brain that encode color categorically have not yet been reliably identified. Here, we used functional MRI adaptation to identify neuronal populations that represent color categories irrespective of metric differences in color. Two colors were successively presented within a block of trials. The two colors were either from the same or different categories (e.g., “blue 1 and blue 2” or “blue 1 and green 1”), and the size of the hue difference was varied. Participants performed a target detection task unrelated to the difference in color. In the middle frontal gyrus of both hemispheres and to a lesser extent, the cerebellum, blood-oxygen level-dependent response was greater for colors from different categories relative to colors from the same category. Importantly, activation in these regions was not modulated by the size of the hue difference, suggesting that neurons in these regions represent color categorically, regardless of metric color difference. Representational similarity analyses, which investigated the similarity of the pattern of activity across local groups of voxels, identified other regions of the brain (including the visual cortex), which responded to metric but not categorical color differences. Therefore, categorical and metric hue differences appear to be coded in qualitatively different ways and in different brain regions. These findings have implications for the long-standing debate on the origin and nature of color categories, and also further our understanding of how color is processed by the brain.

Incongruent abstract stimulus-response bindings result in response interference: Fmri and eeg evidence from visual object classification priming

Stimulus repetition often leads to facilitated processing, resulting in neural decreases (repetition suppression) and faster RTs (repetition priming). Such repetition-related effects have been attributed to the facilitation of repeated cognitive processes and/or the retrieval of previously encoded stimulus–response (S-R) bindings. Although previous research has dissociated these two forms of learning, their interaction in the brain is not fully understood. Utilizing the spatial and temporal resolutions of fMRI and EEG, respectively, we examined a long-lag classification priming paradigm that required response repetitions or reversals at multiple levels of response representation. We found a repetition effect in occipital/temporal cortex (fMRI) that was time-locked to stimulus onset (EEG) and robust to switches in response, together with a repetition effect in inferior pFC (fMRI) that was time-locked to response onset (EEG) and sensitive to switches in response. The response-sensitive effect occurred even when changing from object names (words) to object pictures between repetitions, suggesting that S-R bindings can code abstract representations of stimuli. Most importantly, we found evidence for interference effects when incongruent S-R bindings were retrieved, with increased neural activity in inferior pFC, demonstrating that retrieval of S-R bindings can result in facilitation or interference, depending on the congruency of response between repetitions.