Human Verbal Memory Research Articles

Hotspot of human verbal memory encoding in the left anterior prefrontal cortex.

SummaryBackgroundTreating memory and cognitive deficits requires knowledge about anatomical sites and neural activities to be targeted with particular therapies. Emerging technologies for local brain stimulation offer attractive therapeutic options but need to be applied to target specific neural activities, at distinct times, and in specific brain regions that are critical for memory formation.MethodsThe areas that are critical for successful encoding of verbal memory as well as the underlying neural activities were determined directly in the human brain with intracranial electrophysiological recordings in epilepsy patients. We recorded a broad range of spectral activities across the cortex of 135 patients as they memorised word lists for subsequent free recall.FindingsThe greatest differences in the spectral power between encoding subsequently recalled and forgotten words were found in low theta frequency (3–5 Hz) activities of the left anterior prefrontal cortex. This subsequent memory effect was proportionally greater in the lower frequency bands and in the more anterior cortical regions. We found the peak of this memory signal in a distinct part of the prefrontal cortex at the junction between the Broca's area and the frontal pole. The memory effect in this confined area was significantly higher (Tukey–Kramer test, p<0.05) than in other anatomically distinct areas.InterpretationOur results suggest a focal hotspot of human verbal memory encoding located in the higher-order processing region of the prefrontal cortex, which presents a prospective target for modulating cognitive functions in the human patients. The memory effect provides an electrophysiological biomarker of low frequency neural activities, at distinct times of memory encoding, and in one hotspot location in the human brain.FundingOpen-access datasets were originally collected as part of a BRAIN Initiative project called Restoring Active Memory (RAM) funded by the Defence Advanced Research Project Agency (DARPA). CT, ML, MTK and this research were supported from the First Team grant of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund.

Recognition memory for human motor learning

Motor skill retention is typically measured by asking participants to reproduce previously learned movements from memory. The analog of this retention test (recall memory) in human verbal memory is known to underestimate how much learning is actually retained. Here we asked whether information about previously learned movements, which can no longer be reproduced, is also retained. Following visuomotor adaptation, we used tests of recall that involved reproduction of previously learned movements and tests of recognition in which participants were asked whether a candidate limb displacement, produced by a robot arm held by the subject, corresponded to a movement direction that was experienced during active training. The main finding was that 24h after training, estimates of recognition memory were about twice as accurate as those of recall memory. Thus, there is information about previously learned movements that is not retrieved using recall testing but can be accessed in tests of recognition. We conducted additional tests to assess whether, 24h after learning, recall for previously learned movements could be improved by presenting passive movements as retrieval cues. These tests were conducted immediately prior to recall testing and involved the passive playback of a small number of movements, which were spread across the workspace and included both adapted and baseline movements, without being marked as such. This technique restored recall memory for movements to levels close to those of recognition memory performance. Thus, somatic information may enable retrieval of otherwise inaccessible motor memories.

The Role of Hierarchical Dynamical Functions in Coding for Episodic Memory and Cognition

Behavioral research in human verbal memory function led to the initial definition of episodic memory and semantic memory. A complete model of the neural mechanisms of episodic memory must include the capacity to encode and mentally reconstruct everything that humans can recall from their experience. This article proposes new model features necessary to address the complexity of episodic memory encoding and recall in the context of broader cognition and the functional properties of neurons that could contribute to this broader scope of memory. Many episodic memory models represent individual snapshots of the world with a sequence of vectors, but a full model must represent complex functions encoding and retrieving the relations between multiple stimulus features across space and time on multiple hierarchical scales. Episodic memory involves not only the space and time of an agent experiencing events within an episode but also features shown in neurophysiological data such as coding of speed, direction, boundaries, and objects. Episodic memory includes not only a spatio-temporal trajectory of a single agent but also segments of spatio-temporal trajectories for other agents and objects encountered in the environment consistent with data on encoding the position and angle of sensory features of objects and boundaries. We will discuss potential interactions of episodic memory circuits in the hippocampus and entorhinal cortex with distributed neocortical circuits that must represent all features of human cognition.

Human Verbal Memory Encoding Is Hierarchically Distributed in a Continuous Processing Stream.

Processing of memory is supported by coordinated activity in a network of sensory, association, and motor brain regions. It remains a major challenge to determine where memory is encoded for later retrieval. Here, we used direct intracranial brain recordings from epilepsy patients performing free recall tasks to determine the temporal pattern and anatomical distribution of verbal memory encoding across the entire human cortex. High γ frequency activity (65–115 Hz) showed consistent power responses during encoding of subsequently recalled and forgotten words on a subset of electrodes localized in 16 distinct cortical areas activated in the tasks. More of the high γ power during word encoding, and less power before and after the word presentation, was characteristic of successful recall and observed across multiple brain regions. Latencies of the induced power changes and this subsequent memory effect (SME) between the recalled and forgotten words followed an anatomical sequence from visual to prefrontal cortical areas. Finally, the magnitude of the memory effect was unexpectedly found to be the largest in selected brain regions both at the top and at the bottom of the processing stream. These included the language processing areas of the prefrontal cortex and the early visual areas at the junction of the occipital and temporal lobes. Our results provide evidence for distributed encoding of verbal memory organized along a hierarchical posterior-to-anterior processing stream.

Testing social acoustic memory in rats: Effects of stimulus configuration and long-term memory on the induction of social approach behavior by appetitive 50-kHz ultrasonic vocalizations

Rats emit distinct types of ultrasonic vocalizations (USVs), which serve as situation-dependent affective signals. In appetitive situations, such as rough-and-tumble-play, high-frequency 50-kHz USVs occur, whereas low-frequency 22-kHz USVs can be observed in aversive situations, such as social defeat. USVs serve distinct communicative functions and induce call-specific behavioral responses in the receiver. While aversive 22-kHz USVs serve as alarm calls and induce behavioral inhibition, appetitive 50-kHz USVs have a pro-social communicative function and elicit social approach behavior, supporting the notion that they serve as social contact calls to (re)establish or maintain contact among conspecifics. The aim of the present study was to use the rat’s ability to communicate in the ultrasonic range via high-frequency 50-kHz USVs in order to develop a test for social acoustic memory in rats with relevance for human verbal memory. Verbal learning and memory is among the seven cognitive domains identified as commonly deficient in human schizophrenia patients, but particularly difficult to model. We therefore tested whether the induction of social approach behavior by playback of appetitive 50-kHz USVs is dependent on (1) acoustic stimulus configuration and (2) social long-term memory, and whether (3) social long-term memory effects can be blocked by the administration of scopolamine, a muscarinic acetylcholine antagonist producing amnesia. Results show that social approach behavior in response to playback of natural 50-kHz USVs depends on acoustic stimulus configuration and occurs only when sound energy is concentrated to a critical frequency band in the ultrasonic range. Social approach behavior was detected during the first exposure to playback of 50-kHz USVs, whereas no such response was observed during the second exposure 1week later, indicating a stable memory trace. In contrast, when memory formation was blocked by i.p. administration of scopolamine (0.5mg/kg or 1.5mg/kg) immediately after the first exposure, rats displayed social approach behavior during the second exposure as well. Induction of social approach behavior in response to repeated playback of natural 50-kHz USVs may therefore provide a new and rather unique approach for testing social acoustic memory in rats with relevance to human verbal memory.

Deficits of long-term memory in ecstasy users are related to cognitive complexity of the task

Despite animal evidence that methylenedioxymethamphetamine (ecstasy) causes lasting damage in brain regions related to long-term memory, results regarding human memory performance have been variable. This variability may reflect the cognitive complexity of the memory tasks. However, previous studies have tested only a limited range of cognitive complexity. Furthermore, comparisons across different studies are made difficult by regional variations in ecstasy composition and patterns of use. The objective of this study is to evaluate ecstasy-related deficits in human verbal memory over a wide range of cognitive complexity using subjects drawn from a single geographical population. Ecstasy users were compared to non-drug using controls on verbal tasks with low cognitive complexity (stem completion), moderate cognitive complexity (stem-cued recall and word list learning) and high cognitive complexity (California Verbal Learning Test, Verbal Paired Associates and a novel Verbal Triplet Associates test). Where significant differences were found, both groups were also compared to cannabis users. More cognitively complex memory tasks were associated with clearer ecstasy-related deficits than low complexity tasks. In the most cognitively demanding task, ecstasy-related deficits remained even after multiple learning opportunities, whereas the performance of cannabis users approached that of non-drug using controls. Ecstasy users also had weaker deliberate strategy use than both non-drug and cannabis controls. Results were consistent with the proposal that ecstasy-related memory deficits are more reliable on tasks with greater cognitive complexity. This could arise either because such tasks require a greater contribution from the frontal lobe or because they require greater interaction between multiple brain regions.

Rats’ memory for serially presented flavors: Effects of interstimulus interval and generalization decrement

In four experiments, the effect of sequential exposure to a series of five novel flavors on the subsequent neophobic response of water-deprived rats to those flavors when they were presented simultaneously was examined. After a list-test interval of 30 min and a list-interstimulus interval of 10 sec, the rats generally consumed more of the first and last flavors presented in the initial sequence. This finding was taken to reflect the existence of primacy and recency effects. Experiment 1 provided evidence that successive contamination can occur between flavors in the initial list, making subsequent recognition of later flavors in the list more difficult. However, this effect was overcome by presentation of water between each flavor during the list exposure. Experiments 2 and 4 showed that primacy was not a necessary result of successive contamination in this procedure, by demonstrating that increasing the interstimulus interval between list items decreased the size of the primacy effect. This result suggests that rats’ memory for serially presented items may be controlled by mechanisms different from those typically implicated in the human verbal memory literature. In Experiment 3, the question of whether the testing procedure adopted here could have introduced sources of artifactually produced serialposition effects was explored, but no such influence was found.

Evidence relating human verbal memory to hippocampal N-methyl-D-aspartate receptors.

Studies in rodents and nonhuman primates have linked the activity of N-methyl-D-aspartate (NMDA) receptors within the hippocampus to animals' performance on memory-related tasks. However, whether these receptors are similarly essential for human memory is still an open question. Here we present evidence suggesting that hippocampal NMDA receptors, most likely within the CA1 region, do participate in human verbal memory processes. Words elicit a negative event-related potential (ERP) peaking around 400 ms within the anterior mesial temporal lobe (AMTL-N400). Ketamine, an NMDA-receptor antagonist, reduces the amplitude of the AMTL-N400 (in contrast to other hippocampal potentials) on initial presentation, eliminates the typical AMTL-N400 amplitude reduction with repetition, and leads to significant memory impairment. Of the various hippocampal subfields, only the density of CA1 neurons correlates with the word-related ERPs that are reduced by ketamine. Altogether, our behavioral, anatomical, and electrophysiological results indicate that hippocampal NMDA receptors are involved in human memory.