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Article ; Online: Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus.

Abbaspoor, Saman / Hussin, Ahmed T / Hoffman, Kari L

2023 Volume 12

Abstract: Nested hippocampal oscillations in the rodent give rise to temporal dynamics that may underlie learning, memory, and decision making. Although theta/gamma coupling in rodent CA1 occurs during exploration and sharp-wave ripples emerge in quiescence, it is ...

Abstract	Nested hippocampal oscillations in the rodent give rise to temporal dynamics that may underlie learning, memory, and decision making. Although theta/gamma coupling in rodent CA1 occurs during exploration and sharp-wave ripples emerge in quiescence, it is less clear that these oscillatory regimes extend to primates. We therefore sought to identify correspondences in frequency bands, nesting, and behavioral coupling of oscillations taken from macaque hippocampus. We found that, in contrast to rodent oscillations, theta and gamma frequency bands in macaque CA1 were segregated by behavioral states. In both stationary and freely moving designs, beta2/gamma (15-70 Hz) had greater power during visual search whereas the theta band (3-10 Hz; peak ~8 Hz) dominated during quiescence and early sleep. Moreover, theta-band amplitude was strongest when beta2/slow gamma (20-35 Hz) amplitude was weakest, instead occurring along with higher frequencies (60-150 Hz). Spike-field coherence was most frequently seen in these three bands (3-10 Hz, 20-35 Hz, and 60-150 Hz); however, the theta-band coherence was largely due to spurious coupling during sharp-wave ripples. Accordingly, no intrinsic theta spiking rhythmicity was apparent. These results support a role for beta2/slow gamma modulation in CA1 during active exploration in the primate that is decoupled from theta oscillations. The apparent difference to the rodent oscillatory canon calls for a shift in focus of frequency when considering the primate hippocampus.
MeSH term(s)	Animals ; Macaca ; Hippocampus ; Theta Rhythm ; Learning
Language	English
Publishing date	2023-05-04
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.86548
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Article ; Online: A machine learning toolbox for the analysis of sharp-wave ripples reveals common waveform features across species.

Navas-Olive, Andrea / Rubio, Adrian / Abbaspoor, Saman / Hoffman, Kari L / de la Prida, Liset M

Communications biology

2024 Volume 7, Issue 1, Page(s) 211

Abstract: The study of sharp-wave ripples has advanced our understanding of memory function, and their alteration in neurological conditions such as epilepsy is considered a biomarker of dysfunction. Sharp-wave ripples exhibit diverse waveforms and properties that ...

Abstract	The study of sharp-wave ripples has advanced our understanding of memory function, and their alteration in neurological conditions such as epilepsy is considered a biomarker of dysfunction. Sharp-wave ripples exhibit diverse waveforms and properties that cannot be fully characterized by spectral methods alone. Here, we describe a toolbox of machine-learning models for automatic detection and analysis of these events. The machine-learning architectures, which resulted from a crowdsourced hackathon, are able to capture a wealth of ripple features recorded in the dorsal hippocampus of mice across awake and sleep conditions. When applied to data from the macaque hippocampus, these models are able to generalize detection and reveal shared properties across species. We hereby provide a user-friendly open-source toolbox for model use and extension, which can help to accelerate and standardize analysis of sharp-wave ripples, lowering the threshold for its adoption in biomedical applications.
MeSH term(s)	Animals ; Mice ; Hippocampus ; Macaca ; Machine Learning ; Memory ; Records
Language	English
Publishing date	2024-03-04
Publishing country	England
Document type	Journal Article
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-024-05871-w
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Article ; Online: Retrosplenial and Hippocampal Synchrony during Retrieval of Old Memories in Macaques.

Hussin, Ahmed T / Abbaspoor, Saman / Hoffman, Kari L

The Journal of neuroscience : the official journal of the Society for Neuroscience

2022 Volume 42, Issue 42, Page(s) 7947–7956

Abstract: Memory for events from the distant past relies on multiple brain regions, but little is known about the underlying neural dynamics that give rise to such abilities. We recorded neural activity in the hippocampus and retrosplenial cortex of two female ... ...

Abstract	Memory for events from the distant past relies on multiple brain regions, but little is known about the underlying neural dynamics that give rise to such abilities. We recorded neural activity in the hippocampus and retrosplenial cortex of two female rhesus macaques as they visually selected targets in year-old and newly acquired object-scene associations. Whereas hippocampal activity was unchanging with memory age, the retrosplenial cortex responded with greater magnitude alpha oscillations (10-15 Hz) and greater phase locking to memory-guided eye movements during retrieval of old events. A similar old-memory enhancement was observed in the anterior cingulate cortex but in a beta2/gamma band (28-35 Hz). In contrast, remote retrieval was associated with decreased gamma-band synchrony between the hippocampus and each neocortical area. The increasing retrosplenial alpha oscillation and decreasing hippocampocortical synchrony with memory age may signify a shift in frank memory allocation or, alternatively, changes in selection among distributed memory representations in the primate brain.
MeSH term(s)	Animals ; Female ; Macaca mulatta ; Hippocampus/physiology ; Mental Recall/physiology ; Gyrus Cinguli/physiology ; Brain
Language	English
Publishing date	2022-09-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.0001-22.2022
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Article: A machine learning toolbox for the analysis of sharp-wave ripples reveal common features across species.

Navas-Olive, Andrea / Rubio, Adrian / Abbaspoor, Saman / Hoffman, Kari L / de la Prida, Liset M

bioRxiv : the preprint server for biology

2023

Abstract: The study of sharp-wave ripples (SWRs) has advanced our understanding of memory function, and their alteration in neurological conditions such as epilepsy and Alzheimer's disease is considered a biomarker of dysfunction. SWRs exhibit diverse waveforms ... ...

Abstract	The study of sharp-wave ripples (SWRs) has advanced our understanding of memory function, and their alteration in neurological conditions such as epilepsy and Alzheimer's disease is considered a biomarker of dysfunction. SWRs exhibit diverse waveforms and properties that cannot be fully characterized by spectral methods alone. Here, we describe a toolbox of machine learning (ML) models for automatic detection and analysis of SWRs. The ML architectures, which resulted from a crowdsourced hackathon, are able to capture a wealth of SWR features recorded in the dorsal hippocampus of mice. When applied to data from the macaque hippocampus, these models were able to generalize detection and revealed shared SWR properties across species. We hereby provide a user-friendly open-source toolbox for model use and extension, which can help to accelerate and standardize SWR research, lowering the threshold for its adoption in biomedical applications.
Language	English
Publishing date	2023-07-03
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.02.547382
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Article ; Online: A corollary discharge mediates saccade-related inhibition of single units in mnemonic structures of the human brain.

Katz, Chaim N / Schjetnan, Andrea G P / Patel, Kramay / Barkley, Victoria / Hoffman, Kari L / Kalia, Suneil K / Duncan, Katherine D / Valiante, Taufik A

Current biology : CB

2022 Volume 32, Issue 14, Page(s) 3082–3094.e4

Abstract: Despite the critical link between visual exploration and memory, little is known about how neuronal activity in the human mesial temporal lobe (MTL) is modulated by saccades. Here, we characterize saccade-associated neuronal modulations, unit-by-unit, ... ...

Abstract	Despite the critical link between visual exploration and memory, little is known about how neuronal activity in the human mesial temporal lobe (MTL) is modulated by saccades. Here, we characterize saccade-associated neuronal modulations, unit-by-unit, and contrast them to image onset and to occipital lobe neurons. We reveal evidence for a corollary discharge (CD)-like modulatory signal that accompanies saccades, inhibiting/exciting a unique population of broad-/narrow-spiking units, respectively, before and during saccades and with directional selectivity. These findings comport well with the timing, directional nature, and inhibitory circuit implementation of a CD. Additionally, by linking neuronal activity to event-related potentials (ERPs), which are directionally modulated following saccades, we recontextualize the ERP associated with saccades as a proxy for both the strength of inhibition and saccade direction, providing a mechanistic underpinning for the more commonly recorded saccade-related ERP in the human brain.
MeSH term(s)	Brain ; Humans ; Inhibition, Psychological ; Neurons/physiology ; Photic Stimulation ; Reaction Time/physiology ; Saccades
Language	English
Publishing date	2022-07-01
Publishing country	England
Document type	Journal Article
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2022.06.015
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Article ; Online: Websites about, not for, adolescents? A systematic analysis of online fertility preservation information for adolescent and young adult cancer patients.

Ruiz, Sienna / Mintz, Rachel / Sijecic, Amela / Eggers, Michelle / Hoffman, Aubri S / Woodard, Terri / Bjornard, Kari L / Hoefgen, Holly / Sandheinrich, Taryn / Omurtag, Kenan / Housten, Ashley J

Journal of cancer survivorship : research and practice

2023

Abstract: Purpose: Fertility preservation is an increasingly important topic in adolescent and young adult cancer survivorship, yet treatments remain under-utilized, possibly due to lack of awareness and understanding. The internet is widely used by adolescents ... ...

Abstract	Purpose: Fertility preservation is an increasingly important topic in adolescent and young adult cancer survivorship, yet treatments remain under-utilized, possibly due to lack of awareness and understanding. The internet is widely used by adolescents and young adults and has been proposed to fill knowledge gaps and advance high-quality, more equitable care. As a first step, this study analyzed the quality of current fertility preservation resources online and identified opportunities for improvement. Methods: We conducted a systematic analysis of 500 websites to assess the quality, readability, and desirability of website features, and the inclusion of clinically relevant topics. Results: The majority of the 68 eligible websites were low quality, written at college reading levels, and included few features that younger patients find desirable. Websites mentioned more common fertility preservation treatments than promising experimental treatments, and could be improved with cost information, socioemotional impacts, and other equity-related fertility topics. Conclusions: Currently, the majority of fertility preservation websites are about, but not for, adolescent and young adult patients. High-quality educational websites are needed that address outcomes that matter to teens and young adults, with a priority on solutions that prioritize equity. Implications for cancer survivors: Adolescent and young adult survivors have limited access to high-quality fertility preservation websites that are designed for their needs. There is a need for the development of fertility preservation websites that are clinically comprehensive, written at appropriate reading levels, inclusive, and desirable. We include specific recommendations that future researchers can use to develop websites that could better address AYA populations and improve the fertility preservation decision making process.
Language	English
Publishing date	2023-05-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	2388888-X
ISSN	1932-2267 ; 1932-2259
ISSN (online)	1932-2267
ISSN	1932-2259
DOI	10.1007/s11764-023-01386-1
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Article ; Online: Sharp-Wave Ripples in Primates Are Enhanced near Remembered Visual Objects.

Leonard, Timothy K / Hoffman, Kari L

Current biology : CB

2016 Volume 27, Issue 2, Page(s) 257–262

Abstract: The hippocampus plays an important role in memory for events that are distinct in space and time. One of the strongest, most synchronous neural signals produced by the hippocampus is the sharp-wave ripple (SWR), observed in a variety of mammalian species ...

Abstract	The hippocampus plays an important role in memory for events that are distinct in space and time. One of the strongest, most synchronous neural signals produced by the hippocampus is the sharp-wave ripple (SWR), observed in a variety of mammalian species during offline behaviors, such as slow-wave sleep [1-3] and quiescent waking and pauses in exploration [4-8], leading to long-standing and widespread theories of its contribution to plasticity and memory during these inactive or immobile states [9-14]. Indeed, during sleep and waking inactivity, hippocampal SWRs in rodents appear to support spatial long-term and working memory [4, 15-23], but so far, they have not been linked to memory in primates. More recently, SWRs have been observed during active, visual scene exploration in macaques [24], opening up the possibility that these active-state ripples in the primate hippocampus are linked to memory for objects embedded in scenes. By measuring hippocampal SWRs in macaques during search for scene-contextualized objects, we found that SWR rate increased with repeated presentations. Furthermore, gaze during SWRs was more likely to be near the target object on repeated than on novel presentations, even after accounting for overall differences in gaze location with scene repetition. This proximity bias with repetition occurred near the time of target object detection for remembered targets. The increase in ripple likelihood near remembered visual objects suggests a link between ripples and memory in primates; specifically, SWRs may reflect part of a mechanism supporting the guidance of search based on past experience.
MeSH term(s)	Action Potentials ; Animals ; Female ; Hippocampus/physiology ; Macaca mulatta/physiology ; Mental Recall/physiology ; Visual Perception/physiology
Language	English
Publishing date	2016-12-29
Publishing country	England
Document type	Journal Article
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2016.11.027
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Article ; Online: Sharp-wave ripple features in macaques depend on behavioral state and cell-type specific firing.

Hussin, Ahmed T / Leonard, Timothy K / Hoffman, Kari L

Hippocampus

2018 Volume 30, Issue 1, Page(s) 50–59

Abstract: Sharp-wave ripples (SWRs) are spontaneous, synchronized neural population events in the hippocampus widely thought to play a role in memory consolidation and retrieval. They occur predominantly in sleep and quiet immobility, and in primates, they also ... ...

Abstract	Sharp-wave ripples (SWRs) are spontaneous, synchronized neural population events in the hippocampus widely thought to play a role in memory consolidation and retrieval. They occur predominantly in sleep and quiet immobility, and in primates, they also appear during active visual exploration. Typical measures of SWRs in behaving rats include changes in the rate of occurrence, or in the incidence of specific neural ensemble activity contained within the categorical SWR event. Much less is known about the relevance of spatiotemporal SWR features, though they may index underlying activity of specific cell types including ensemble-specific internally generated sequences. Furthermore, changes in SWR features during active exploratory states are unknown. In this study, we recorded hippocampal local-field potentials and single-units during periods of quiescence and as macaques performed a memory-guided visual search task. We observed that (a) ripples during quiescence have greater amplitudes and larger postripple waves (PRW) compared to those in task epochs, and (b) during "remembered" trials, ripples have larger amplitudes than during "forgotten" trials, with no change in duration or PRWs. We further found that spiking activity influences SWR features as a function of cell type and ripple timing. As expected, larger ripple amplitudes were associated with putative pyramidal or putative basket interneuron (IN) activity, even when the spikes in question exceed the duration of the ripple. In contrast, the PRW was attenuated with activity from low firing rate cells and enhanced with activity from high firing rate cells, with putative IN spikes during ripples leading to the most prominent PRW peaks. The selective changes in SWR features as a function of time window, cell type, and cognitive/vigilance states suggest that this mesoscopic field event can offer additional information about the local network and animal's state than would be appreciated from SWR event rates alone.
MeSH term(s)	Action Potentials/physiology ; Animals ; Brain Waves/physiology ; Female ; Hippocampus/physiology ; Interneurons/physiology ; Macaca mulatta ; Nerve Net/physiology ; Neurons/physiology ; Photic Stimulation ; Recognition, Psychology/physiology
Language	English
Publishing date	2018-11-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1074352-2
ISSN	1098-1063 ; 1050-9631
ISSN (online)	1098-1063
ISSN	1050-9631
DOI	10.1002/hipo.23046
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Article ; Online: Long-term memory and hippocampal function support predictive gaze control during goal-directed search.

Yoo, Sang-Ah / Rosenbaum, R Shayna / Tsotsos, John K / Fallah, Mazyar / Hoffman, Kari L

Journal of vision

2020 Volume 20, Issue 5, Page(s) 10

Abstract: Eye movements during visual search change with prior experience for search stimuli. Previous studies measured these gaze effects shortly after initial viewing, typically during free viewing; it remains open whether the effects are preserved across long ... ...

Abstract	Eye movements during visual search change with prior experience for search stimuli. Previous studies measured these gaze effects shortly after initial viewing, typically during free viewing; it remains open whether the effects are preserved across long delays and for goal-directed search, and which memory system guides gaze. In Experiment 1, we analyzed eye movements of healthy adults viewing novel and repeated scenes while searching for a scene-embedded target. The task was performed across different time points to examine the repetition effects in long-term memory, and memory types were grouped based on explicit recall of targets. In Experiment 2, an amnesic person with bilateral extended hippocampal damage and the age-matched control group performed the same task with shorter intervals to determine whether or not the repetition effects depend on hippocampal function. When healthy adults explicitly remembered repeated target-scene pairs, search time and fixation duration decreased, and gaze was directed closer to the target region, than when they forgot targets. These effects were seen even after a one-month delay from their initial viewing, suggesting the effects are associated with long-term, explicit memory. Saccadic amplitude was not strongly modulated by scene repetition or explicit recall of targets. The amnesic person did not show explicit recall or implicit repetition effects, whereas his control group showed similar patterns to those seen in Experiment 1. The results reveal several aspects of gaze control that are influenced by long-term memory. The dependence of gaze effects on medial temporal lobe integrity support a role for this region in predictive gaze control.
MeSH term(s)	Adult ; Eye Movements ; Female ; Fixation, Ocular ; Goals ; Hippocampus/physiology ; Humans ; Male ; Memory, Long-Term ; Mental Recall ; Young Adult
Language	English
Publishing date	2020-05-26
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2106064-2
ISSN	1534-7362 ; 1534-7362
ISSN (online)	1534-7362
ISSN	1534-7362
DOI	10.1167/jov.20.5.10
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Article ; Online: Hippocampal gamma-band Synchrony and pupillary responses index memory during visual search.

Montefusco-Siegmund, Rodrigo / Leonard, Timothy K / Hoffman, Kari L

Hippocampus

2017 Volume 27, Issue 4, Page(s) 425–434

Abstract: Memory for scenes is supported by the hippocampus, among other interconnected structures, but the neural mechanisms related to this process are not well understood. To assess the role of the hippocampus in memory-guided scene search, we recorded local ... ...

Abstract	Memory for scenes is supported by the hippocampus, among other interconnected structures, but the neural mechanisms related to this process are not well understood. To assess the role of the hippocampus in memory-guided scene search, we recorded local field potentials and multiunit activity from the hippocampus of macaques as they performed goal-directed search tasks using natural scenes. We additionally measured pupil size during scene presentation, which in humans is modulated by recognition memory. We found that both pupil dilation and search efficiency accompanied scene repetition, thereby indicating memory for scenes. Neural correlates included a brief increase in hippocampal multiunit activity and a sustained synchronization of unit activity to gamma band oscillations (50-70 Hz). The repetition effects on hippocampal gamma synchronization occurred when pupils were most dilated, suggesting an interaction between aroused, attentive processing and hippocampal correlates of recognition memory. These results suggest that the hippocampus may support memory-guided visual search through enhanced local gamma synchrony. © 2016 Wiley Periodicals, Inc.
Language	English
Publishing date	2017-04
Publishing country	United States
Document type	Journal Article
ZDB-ID	1074352-2
ISSN	1098-1063 ; 1050-9631
ISSN (online)	1098-1063
ISSN	1050-9631
DOI	10.1002/hipo.22702
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