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Neurons in the medial temporal lobe (MTL), a critical area for declarative memory, have been shown to change their tuning in associative learning tasks. Yet, it is unclear how durable these neuronal representations are and if they outlast the execution of the task. To address this issue, we studied the responses of MTL neurons in neurosurgical patients to known concepts (people and places). Using association scores provided by the patients and a web-based metric, here we show that whenever MTL neurons respond to more than one concept, these concepts are typically related. Furthermore, the degree of association between concepts could be successfully predicted based on the neurons’ response patterns. These results provide evidence for a long-term involvement of MTL neurons in the representation of durable associations, a hallmark of human declarative memory. Neurons in the medial temporal lobe change their firing patterns as people learn to pair items together, yet it is unclear if this pairing lasts. Here, authors find that single medial temporal lobe neurons in humans tend to respond similarly to items that are closely conceptually related.

Despite the compelling contribution of the study of event related potentials (ERPs) and eye movements to cognitive neuroscience, these two approaches have largely evolved independently. We designed an eye-movement visual search paradigm that allowed us to concurrently record EEG and eye movements while subjects were asked to find a hidden target face in a crowded scene with distractor faces. Fixation event-related potentials (fERPs) to target and distractor stimuli showed the emergence of robust sensory components associated with the perception of stimuli and cognitive components associated with the detection of target faces. We compared those components with the ones obtained in a control task at fixation: qualitative similarities as well as differences in terms of scalp topography and latency emerged between the two. By using single trial analyses, fixations to target and distractors could be decoded from the EEG signals above chance level in 11 out of 12 subjects. Our results show that EEG signatures related to cognitive behavior develop across spatially unconstrained exploration of natural scenes and provide a first step towards understanding the mechanisms of target detection during natural search. •Robust cognitive fixation-related potentials emerge during natural scene exploration.•The potentials resemble in some aspects classical ERPs obtained under fixed-gaze.•Target identity was distinguished using single-trial analysis in 11/12 subjects.•Our results pave the way for future EEG experiments in ecological scenarios.

Besides decades of research showing the role of the medial temporal lobe (MTL) in memory and the encoding of associations, the neural substrates underlying these functions remain unknown. We identified single neurons in the human MTL that responded to multiple and, in most cases, associated stimuli. We observed that most of these neurons exhibit no differences in their spike and local field potential (LFP) activity associated with the individual response-eliciting stimuli. In addition, LFP responses in the theta band preceded single neuron responses by ~70 ms, with the single trial phase providing fine tuning of the spike response onset. We postulate that the finding of similar neuronal responses to associated items provides a simple and flexible way of encoding memories in the human MTL, increasing the effective capacity for memory storage and successful retrieval. In this work, the authors recorded single neurons and field potentials from the human medial temporal lobe (MTL) and show indistinguishable responses to associated stimuli. This coding mechanism provides a simple and flexible way of encoding memories in the human MTL.

In real-life scenarios, individuals frequently engage in tasks that involve searching for one of the distinct items stored in memory. This combined process of visual search and memory search is known as hybrid search. To date, most hybrid search studies have been restricted to average observers looking for previously well-memorized targets in blank backgrounds. We investigated the effects of context and the role of memory in hybrid search by modifying the task's memorization phase to occur in all-new single trials. In addition, we aimed to assess how individual differences in visual working memory capacity and inhibitory control influence performance during hybrid search. In an online experiment, 110 participants searched for potential targets in images with and without context. A change detection and go/no-go task were also performed to measure working memory capacity and inhibitory control, respectively. We show that, in target present trials, the main hallmarks of hybrid search remain present, with a linear relationship between reaction time and visual set size and a logarithmic relationship between reaction time and memory set size. These behavioral results can be reproduced by using a simple drift-diffusion model. Finally, working memory capacity did not predict most search performance measures. Inhibitory control, when relationships were significant, could account for only a small portion of the variability in the data. This study provides insights into the effects of context and individual differences on search efficiency and termination.

A population of human hippocampal neurons has shown responses to individual concepts (e.g., Jennifer Aniston) that generalize to different instances of the concept. However, recordings from the rodent hippocampus suggest an important function of these neurons is their ability to discriminate overlapping representations, or pattern separate, a process that may facilitate discrimination of similar events for successful memory. In the current study, we explored whether human hippocampal neurons can also demonstrate the ability to discriminate between overlapping representations and whether this selectivity could be directly related to memory performance. We show that among medial temporal lobe (MTL) neurons, certain populations of neurons are selective for a previously studied (target) image in that they show a significant decrease in firing rate to very similar (lure) images.We found that a greater proportion of these neurons can be found in the hippocampus compared with other MTL regions, and that memory for individual items is correlated to the degree of selectivity of hippocampal neurons responsive to those items. Moreover, a greater proportion of hippocampal neurons showed selective firing for target images in good compared with poor performers, with overall memory performance correlated with hippocampal selectivity. In contrast, selectivity in other MTL regions was not associated with memory performance. These findings show that a substantial proportion of human hippocampal neurons encode specific memories that support the discrimination of overlapping representations. These results also provide previously unidentified evidence consistent with a unique role of the human hippocampus in orthogonalization of representations in declarative memory.

Exposure to loud sound causes cochlear damage resulting in hearing loss and tinnitus. Tinnitus has been related to hyperactivity in the central auditory pathway occurring weeks after loud sound exposure. However, central excitability changes concomitant to hearing loss and preceding those periods of hyperactivity, remain poorly explored. Here we investigate mechanisms contributing to excitability changes in the dorsal cochlear nucleus (DCN) shortly after exposure to loud sound that produces hearing loss. We show that acoustic overexposure alters synaptic transmission originating from the auditory and the multisensory pathway within the DCN in different ways. A reduction in the number of myelinated auditory nerve fibers leads to a reduced maximal firing rate of DCN principal cells, which cannot be restored by increasing auditory nerve fiber recruitment. In contrast, a decreased membrane resistance of DCN granule cells (multisensory inputs) leads to a reduced maximal firing rate of DCN principal cells that is overcome when additional multisensory fibers are recruited. Furthermore, gain modulation by inhibitory synaptic transmission is disabled in both auditory and multisensory pathways. These cellular mechanisms that contribute to decreased cellular excitability in the central auditory pathway are likely to represent early neurobiological markers of hearing loss and may suggest interventions to delay or stop the development of hyperactivity that has been associated with tinnitus.

Visual search involves a sequence or routine of unitary operations (i.e. fixations) embedded in a larger mental global program. The process can indeed be seen as a program based on a while loop (while the target is not found), a conditional construct (whether the target is matched or not based on specific recognition algorithms) and a decision making step to determine the position of the next searched location based on existent evidence. Recent developments in our ability to co-register brain scalp potentials (EEG) during free eye movements has allowed investigating brain responses related to fixations (fixation-Related Potentials; fERPs), including the identification of sensory and cognitive local EEG components linked to individual fixations. However, the way in which the mental program guiding the search unfolds has not yet been investigated. We performed an EEG and eye tracking co-registration experiment in which participants searched for a target face in natural images of crowds. Here we show how unitary steps of the program are encoded by specific local target detection signatures and how the positioning of each unitary operation within the global search program can be pinpointed by changes in the EEG signal amplitude as well as the signal power in different frequency bands. By simultaneously studying brain signatures of unitary operations and those occurring during the sequence of fixations, our study sheds light into how local and global properties are combined in implementing visual routines in natural tasks.

Imaging, electrophysiological, and lesion studies have shown a relationship between the parahippocampal cortex (PHC) and the processing of spatial scenes. Our present knowledge of PHC, however, is restricted to the macroscopic properties and dynamics of bulk tissue; the behavior and selectivity of single parahippocampal neurons remains largely unknown. In this study, we analyzed responses from 630 parahippocampal neurons in 24 neurosurgical patients during visual stimulus presentation. We found a spatially clustered subpopulation of scene-selective units with an associated event-related field potential. These units form a population code that is more distributed for scenes than for other stimulus categories, and less sparse than elsewhere in the medial temporal lobe. Our electrophysiological findings provide insight into how individual units give rise to the population response observed with functional imaging in the parahippocampal place area.

Episodic memories are long lasting and full of detail, yet imperfect and malleable. We quantitatively evaluated recollection of short audiovisual segments from movies as a proxy to real-life memory formation in 161 subjects at 15 minutes up to a year after encoding. Memories were reproducible within and across individuals, showed the typical decay with time elapsed between encoding and testing, were fallible yet accurate, and were insensitive to low-level stimulus manipulations but sensitive to high-level stimulus properties. Remarkably, memorability was also high for single movie frames, even one year post-encoding. To evaluate what determines the efficacy of long-term memory formation, we developed an extensive set of content annotations that included actions, emotional valence, visual cues and auditory cues. These annotations enabled us to document the content properties that showed a stronger correlation with recognition memory and to build a machine-learning computational model that accounted for episodic memory formation in single events for group averages and individual subjects with an accuracy of up to 80%. These results provide initial steps towards the development of a quantitative computational theory capable of explaining the subjective filtering steps that lead to how humans learn and consolidate memories.

Early access to categorical visual information plays an important role in real-world behaviour. Under fixed-gaze conditions, there are well-established electrophysiological signatures of categorical processing like the N170 EEG component. Here we aimed to study how the sensitivity to category information extends to a free viewing paradigm and consider how ecologically-relevant variables such as the particular task performed influence the brain activity. We co-registered EEG and eye-tracking to investigate fixation-related potentials to pictures of different categories during visual search and exploration. Participants were asked to observe or search for one target from an array of faces and objects embedded in random noise. We applied a deconvolution analysis approach to estimate the contribution of the different elements embedded in the task. Consistent with classical fixed-gaze experiments and a handful of free viewing studies, we found a robust categorial effect in occipital and occipitotemporal electrodes. We also report a task effect, which was reflected by a negative occipital activation and a positive frontal activation of the estimates. To further investigate the dynamics along the trial, we defined a trial progression score and found significant effects of trial progression, and the interaction between the trial progression and task effects. Overall, these results generalise the characterisation of early visual face processing to a wider range of experiments and show how a suitable analysis approach allows to discern among multiple neural contributions to the signal, preserving key attributes of real-world tasks. Competing Interest Statement The authors have declared no competing interest.