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1.
PLoS Comput Biol ; 19(12): e1011727, 2023 Dec.
Article in English | MEDLINE | ID: mdl-38117859

ABSTRACT

Empirical evidence shows that memories that are frequently revisited are easy to recall, and that familiar items involve larger hippocampal representations than less familiar ones. In line with these observations, here we develop a modelling approach to provide a mechanistic understanding of how hippocampal neural assemblies evolve differently, depending on the frequency of presentation of the stimuli. For this, we added an online Hebbian learning rule, background firing activity, neural adaptation and heterosynaptic plasticity to a rate attractor network model, thus creating dynamic memory representations that can persist, increase or fade according to the frequency of presentation of the corresponding memory patterns. Specifically, we show that a dynamic interplay between Hebbian learning and background firing activity can explain the relationship between the memory assembly sizes and their frequency of stimulation. Frequently stimulated assemblies increase their size independently from each other (i.e. creating orthogonal representations that do not share neurons, thus avoiding interference). Importantly, connections between neurons of assemblies that are not further stimulated become labile so that these neurons can be recruited by other assemblies, providing a neuronal mechanism of forgetting.


Subject(s)
Learning , Reinforcement, Psychology , Learning/physiology , Mental Recall/physiology , Neurons/physiology , Hippocampus/physiology , Neuronal Plasticity/physiology , Models, Neurological
2.
Nat Commun ; 14(1): 5661, 2023 09 13.
Article in English | MEDLINE | ID: mdl-37704636

ABSTRACT

Faces are critical for social interactions and their recognition constitutes one of the most important and challenging functions of the human brain. While neurons responding selectively to faces have been recorded for decades in the monkey brain, face-selective neural activations have been reported with neuroimaging primarily in the human midfusiform gyrus. Yet, the cellular mechanisms producing selective responses to faces in this hominoid neuroanatomical structure remain unknown. Here we report single neuron recordings performed in 5 human subjects (1 male, 4 females) implanted with intracerebral microelectrodes in the face-selective midfusiform gyrus, while they viewed pictures of familiar and unknown faces and places. We observed similar responses to faces and places at the single cell level, but a significantly higher number of neurons responding to faces, thus offering a mechanistic account for the face-selective activations observed in this region. Although individual neurons did not respond preferentially to familiar faces, a population level analysis could consistently determine whether or not the faces (but not the places) were familiar, only about 50 ms after the initial recognition of the stimuli as faces. These results provide insights into the neural mechanisms of face processing in the human brain.


Subject(s)
Endocrine Glands , Facial Recognition , Female , Humans , Male , Neurons , Brain , Cerebral Cortex
3.
Hippocampus ; 33(5): 616-634, 2023 05.
Article in English | MEDLINE | ID: mdl-36965048

ABSTRACT

We describe an integrative model that encodes associations between related concepts in the human hippocampal formation, constituting the skeleton of episodic memories. The model, based on partially overlapping assemblies of "concept cells," contrast markedly with the well-established notion of pattern separation, which relies on conjunctive, context dependent single neuron responses, instead of the invariant, context independent responses found in the human hippocampus. We argue that the model of partially overlapping assemblies is better suited to cope with memory capacity limitations, that the finding of different types of neurons and functions in this area is due to a flexible and temporary use of the extraordinary machinery of the hippocampus to deal with the task at hand, and that only information that is relevant and frequently revisited will consolidate into long-term hippocampal representations, using partially overlapping assemblies. Finally, we propose that concept cells are uniquely human and that they may constitute the neuronal underpinnings of cognitive abilities that are much further developed in humans compared to other species.


Subject(s)
Hippocampus , Memory, Episodic , Humans , Hippocampus/physiology , Neurons/physiology
4.
Trends Cogn Sci ; 25(11): 923-924, 2021 11.
Article in English | MEDLINE | ID: mdl-34598878
5.
J Neurosci Methods ; 360: 109230, 2021 08 01.
Article in English | MEDLINE | ID: mdl-34052290

ABSTRACT

BACKGROUND: There is an active debate about the mechanism underlying the generation of event-related potentials, and, particularly, whether these are generated by additive components, independent of the background EEG, or the phase-resetting of ongoing oscillations. METHOD: We present a new metric to evaluate trial-by-trial covariations of successive ERP components. Our main assumption is that if two successive ERP components are generated by phase-resetting of a unitary oscillation, they should be time-locked to each other and their single-trial latencies should covary. In contrast, if the components are generated by independent additive components, single-trial latency covariations should not be observed. To quantify the covariance between the single-trial latencies, we define a metric based on latency-corrected averages, which we applied to both simulated and real ERPs. RESULTS: For the simulated data, there was a clear distinction in latency covariation between the ERPs generated with unitary phase-resetting versus additive models. For real visual and auditory ERPs, we observed a lack of latency covariation of successive components. COMPARISON WITH EXISTING METHODS: The new metric is complementary to other approaches to study the mechanisms underlying ERP generation, and does not suffer from potential caveats due to filtering artifacts. Moreover, the method proved to be more sensitive than another estimation of single-trial latency covariations using the cross-correlation function. CONCLUSION: The observed lack of latency covariation shows the presence of parallel, independent processing within each cortical sensory pathway.


Subject(s)
Electroencephalography , Evoked Potentials , Artifacts , Humans , Reaction Time
6.
Trends Cogn Sci ; 25(6): 425-426, 2021 06.
Article in English | MEDLINE | ID: mdl-33820659

Subject(s)
Hippocampus , Memory , Humans
7.
Trends Cogn Sci ; 24(12): 994-1007, 2020 12.
Article in English | MEDLINE | ID: mdl-33162337

ABSTRACT

Pattern separation is a basic principle of neuronal coding that precludes memory interference in the hippocampus. Its existence is supported by numerous theoretical, computational, and experimental findings in different species. However, I argue that recent evidence from single-neuron recordings suggests that pattern separation may not be present in the human hippocampus and that memories are instead coded by the coactivation of invariant and context-independent engrams. This alternative model prompts a reassessment of the definition of episodic memory and its distinction from semantic memory. Furthermore, I propose that a lack of pattern separation in memory coding may have profound implications that could explain cognitive abilities that are uniquely developed in humans, such as our power of generalization and of creative and abstract thinking.


Subject(s)
Hippocampus , Memory, Episodic , Hippocampus/physiology , Humans , Neurons/physiology
9.
Curr Biol ; 30(6): 1152-1159.e3, 2020 03 23.
Article in English | MEDLINE | ID: mdl-32142694

ABSTRACT

Experimental findings show the ubiquitous presence of graded responses and tuning curves in the neocortex, particularly in visual areas [1-15]. Among these, inferotemporal-cortex (IT) neurons respond to complex visual stimuli, but differences in the neurons' responses can be used to distinguish the stimuli eliciting the responses [8, 9, 16-18]. The IT projects directly to the medial temporal lobe (MTL) [19], where neurons respond selectively to different pictures of specific persons and even to their written and spoken names [20-22]. However, it is not clear whether this is done through a graded coding, as in the neocortex, or a truly invariant code, in which the response-eliciting stimuli cannot be distinguished from each other. To address this issue, we recorded single neurons during the repeated presentation of different stimuli (pictures and written and spoken names) corresponding to the same persons. Using statistical tests and a decoding approach, we found that only in a minority of cases can the different pictures of a given person be distinguished from the neurons' responses and that in a larger proportion of cases, the responses to the pictures were different to the ones to the written and spoken names. We argue that MTL neurons tend to lack a representation of sensory features (particularly within a sensory modality), which can be advantageous for the memory function attributed to this area [23-25], and that a full representation of memories is given by a combination of mostly invariant coding in the MTL with a representation of sensory features in the neocortex.


Subject(s)
Hippocampus/physiology , Neocortex/physiology , Neurons/physiology , Pattern Recognition, Visual/physiology , Temporal Lobe/physiology , Adult , Argentina , Brain Mapping , Humans , Male , Middle Aged , Single-Cell Analysis , Young Adult
10.
Cell ; 179(5): 1015-1032, 2019 Nov 14.
Article in English | MEDLINE | ID: mdl-31730847

ABSTRACT

We describe single-neuron recordings in the human hippocampal formation, performed in epileptic patients for clinical reasons, and highlight their advantages, challenges, and limitations compared with non-invasive recordings in humans and invasive recordings in animals. We propose a unified framework to explain different findings-responses to novel stimuli, spatial locations, and specific concepts-linking the rodent and human literature regarding the function of the hippocampal formation. Moreover, we propose a model of how memories are encoded in this area, suggesting that the context-independent, invariant coding by concept cells may provide a uniquely human neural mechanism underlying memory representations.


Subject(s)
Memory/physiology , Neurons/physiology , Action Potentials/physiology , Humans , Memory Consolidation/physiology , Models, Neurological , Reaction Time/physiology
12.
PLoS One ; 14(1): e0211468, 2019.
Article in English | MEDLINE | ID: mdl-30699188

ABSTRACT

Temporal regularities in the environment are often learned implicitly. In an auditory target-detection paradigm using EEG, Jongsma and colleagues (2006) showed that the neural response to these implicit regularities results in a reduction of the P3-N2 complex. Here, we utilized the same paradigm, this time in both young and old participants, to determine if this EEG signature of implicit learning was altered with age. Behaviorally, both groups of participants showed similar benefits for the presence of temporal regularity, with faster and more accurate responses given when the auditory targets were presented in a temporally regular vs. random pattern. In the brain, the younger adults showed the expected decrease in amplitude of this complex for regular compared to irregular trials. Older adults, in contrast, showed no difference in the amplitude of the P3-N2 complex between the irregular and regular condition. These data suggest that, although auditory implicit learning may be behaviorally spared in aging, older adults are not using the same neural substrates as younger adults to achieve this.


Subject(s)
Aging/physiology , Auditory Perception/physiology , Auditory Threshold/physiology , Learning/physiology , Neural Pathways/physiology , Reaction Time , Adult , Aged , Female , Humans , Male , Middle Aged , Neuropsychological Tests , Young Adult
13.
Nat Commun ; 9(1): 4372, 2018 10 22.
Article in English | MEDLINE | ID: mdl-30348996

ABSTRACT

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.


Subject(s)
Neurons/metabolism , Temporal Lobe/physiology , Action Potentials/physiology , Adult , Electroencephalography , Female , Hippocampus/cytology , Hippocampus/metabolism , Humans , Magnetic Resonance Imaging , Male , Middle Aged
14.
J Neurophysiol ; 120(4): 1859-1871, 2018 10 01.
Article in English | MEDLINE | ID: mdl-29995603

ABSTRACT

The most widely used spike-sorting algorithms are semiautomatic in practice, requiring manual tuning of the automatic solution to achieve good performance. In this work, we propose a new fully automatic spike-sorting algorithm that can capture multiple clusters of different sizes and densities. In addition, we introduce an improved feature selection method, by using a variable number of wavelet coefficients, based on the degree of non-Gaussianity of their distributions. We evaluated the performance of the proposed algorithm with real and simulated data. With real data from single-channel recordings, in ~95% of the cases the new algorithm replicated, in an unsupervised way, the solutions obtained by expert sorters, who manually optimized the solution of a previous semiautomatic algorithm. This was done while maintaining a low number of false positives. With simulated data from single-channel and tetrode recordings, the new algorithm was able to correctly detect many more neurons compared with previous implementations and also compared with recently introduced algorithms, while significantly reducing the number of false positives. In addition, the proposed algorithm showed good performance when tested with real tetrode recordings. NEW & NOTEWORTHY We propose a new fully automatic spike-sorting algorithm, including several steps that allow the selection of multiple clusters of different sizes and densities. Moreover, it defines the dimensionality of the feature space in an unsupervised way. We evaluated the performance of the algorithm with real and simulated data, from both single-channel and tetrode recordings. The proposed algorithm was able to outperform manual sorting from experts and other recent unsupervised algorithms.


Subject(s)
Algorithms , Electroencephalography/methods , Animals , Cortical Excitability , Electrodes/standards , Electroencephalography/instrumentation , Humans , Sensitivity and Specificity , Software
15.
J Neurosci Methods ; 296: 12-22, 2018 02 15.
Article in English | MEDLINE | ID: mdl-29277720

ABSTRACT

BACKGROUND: Over 90 years after its first recording, scalp electroencephalography (EEG) remains one of the most widely used techniques in human neuroscience research, in particular for the study of event-related potentials (ERPs). However, because of its low signal-to-noise ratio, extracting useful information from these signals continues to be a hard-technical challenge. Many studies focus on simple properties of the ERPs such as peaks, latencies, and slopes of signal deflections. NEW METHOD: To overcome these limitations, we developed the Wavelet-Information method which uses wavelet decomposition, information theory, and a quantification based on single-trial decoding performance to extract information from evoked responses. RESULTS: Using simulations and real data from four experiments, we show that the proposed approach outperforms standard supervised analyses based on peak amplitude estimation. Moreover, the method can extract information using the raw data from all recorded channels using no a priori knowledge or pre-processing steps. COMPARISON WITH EXISTING METHOD(S): We show that traditional approaches often disregard important features of the signal such as the shape of EEG waveforms. Also, other approaches often require some form of a priori knowledge for feature selection and lead to problems of multiple comparisons. CONCLUSIONS: This approach offers a new and complementary framework to design experiments that go beyond the traditional analyses of ERPs. Potentially, it allows a wide usage beyond basic research; such as for clinical diagnosis, brain-machine interfaces, and neurofeedback applications requiring single-trial analyses.


Subject(s)
Electroencephalography/methods , Evoked Potentials , Signal Processing, Computer-Assisted , Auditory Perception/physiology , Brain/physiology , Computer Simulation , Electrodes, Implanted , Humans , Information Theory , Pattern Recognition, Automated/methods , Pattern Recognition, Physiological/physiology , Recognition, Psychology/physiology , Supervised Machine Learning , Visual Perception/physiology , Wavelet Analysis
16.
Cell ; 169(6): 975-977, 2017 06 01.
Article in English | MEDLINE | ID: mdl-28575674

ABSTRACT

How individual faces are encoded by neurons in high-level visual areas has been a subject of active debate. An influential model is that neurons encode specific faces. However, Chang and Tsao conclusively show that, instead, these neurons encode features along specific axes, which explains why they were previously found to respond to apparently different faces.


Subject(s)
Face , Neurons , Humans
17.
Psychophysiology ; 54(8): 1138-1150, 2017 Aug.
Article in English | MEDLINE | ID: mdl-28444975

ABSTRACT

Given the higher chance to recognize attended compared to unattended stimuli, the specific neural correlates of these two processes, attention and awareness, tend to be intermingled in experimental designs. In this study, we dissociated the neural correlates of conscious face perception from the effects of visual attention. To do this, we presented faces at the threshold of awareness and manipulated attention through the use of exogenous prestimulus cues. We show that the N170 component, a scalp EEG marker of face perception, was modulated independently by attention and by awareness. An earlier P1 component was not modulated by either of the two effects and a later P3 component was indicative of awareness but not of attention. These claims are supported by converging evidence from (a) modulations observed in the average evoked potentials, (b) correlations between neural and behavioral data at the single-subject level, and (c) single-trial analyses. Overall, our results show a clear dissociation between the neural substrates of attention and awareness. Based on these results, we argue that conscious face perception is triggered by a boost in face-selective cortical ensembles that can be modulated by, but are still independent from, visual attention.


Subject(s)
Attention/physiology , Cerebral Cortex/physiology , Evoked Potentials, Visual/physiology , Facial Recognition/physiology , Visual Perception/physiology , Adolescent , Adult , Electroencephalography , Female , Humans , Male , Photic Stimulation , Young Adult
18.
Curr Biol ; 27(7): 1026-1032, 2017 Apr 03.
Article in English | MEDLINE | ID: mdl-28318972

ABSTRACT

Working memory is an essential component of human cognition. Persistent activity related to working memory has been reported in many brain areas, including the inferior temporal and prefrontal cortex [1-8]. The medial temporal lobe (MTL) contains "concept cells" that respond invariantly to specific individuals or places whether presented as images, text, or speech [9, 10]. It is unknown, however, whether the MTL also participates in working memory processes. We thus sought to determine whether human MTL neurons respond to images held in working memory. We recorded from patients with chronically intractable epilepsy as they performed a task that required them to remember three or four sequentially presented pictures across a brief delay. 48% of visually selective neurons continued to carry image-specific information after image offset, but most ceased to encode previously presented images after a subsequent presentation of a different image. However, 8% of visually selective neurons encoded previously presented images during a final maintenance period, despite presentation of further images in the intervening interval. Population activity of stimulus-selective neurons predicted behavioral outcome in terms of correct and incorrect responses. These findings indicate that the MTL is part of a brain-wide network for working memory.


Subject(s)
Memory, Short-Term/physiology , Mental Recall , Neurons/physiology , Temporal Lobe/physiology , Epilepsy , Humans
19.
Proc Natl Acad Sci U S A ; 114(5): 1153-1158, 2017 01 31.
Article in English | MEDLINE | ID: mdl-28096381

ABSTRACT

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.


Subject(s)
Environment , Evoked Potentials, Visual , Neurons/physiology , Parahippocampal Gyrus/cytology , Space Perception/physiology , Visual Perception/physiology , Animals , Entorhinal Cortex/physiology , Hippocampus/physiology , Humans , Parahippocampal Gyrus/physiology , Photic Stimulation
20.
Nat Commun ; 7: 13408, 2016 11 15.
Article in English | MEDLINE | ID: mdl-27845773

ABSTRACT

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.


Subject(s)
Association Learning/physiology , Brain/physiopathology , Epilepsy/physiopathology , Memory/physiology , Algorithms , Brain Mapping , Electrodes , Electrophysiology , Humans , Magnetic Resonance Imaging , Models, Neurological , Neurons/physiology , Photic Stimulation , Temporal Lobe/physiopathology
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