Hippocampal-like network dynamics underlie avian sharp wave-ripples

Yeganegi, Hamed; Luksch, Harald; Ondracek, Janie M.

doi:10.1101/825075

Cited by 8 publications

(5 citation statements)

References 38 publications

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“…Similar activity has been observed in fish [1], reptiles [11] and birds [12], indicating that the brain circuits involved in their generation are evolutionary old. The existence of SPW/Rs in non-mammalian species remains, however, a controversial subject [1,12].…”

Section: Introductionsupporting

confidence: 67%

High-frequency oscillations and replay in a two-population model of hippocampal region CA1

Braun

Memmesheimer

2021

Preprint

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Hippocampal sharp wave/ripple oscillations are a prominent pattern of collective activity, which consists of a strong overall increase of activity with onmodulated (140 − 200 Hz) ripple oscillations. Despite its prominence and its experimentally demonstrated importance for memory consolidation, the mechanisms underlying its generation are to date not understood. Several models assume that recurrent networks of inhibitory cells alone can explain the generation and main characteristics of the ripple oscillations. Recent experiments, however, indicate that in addition to inhibitory basket cells, the pattern requires in vivo the activity of the local population of excitatory pyramidal cells. Here we study a model for networks in the hippocampal region CA1 incorporating such a local excitatory population of pyramidal neurons and investigate its ability to generate ripple oscillations using extensive simulations. We find that with biologically plausible values for single neuron, synapse and connectivity parameters, random connectivity and absent strong feedforward drive to the inhibitory population, oscillation patterns similar to in vivo sharp wave/ripples can only be generated if excitatory cell spiking is triggered by short pulses of external excitation. Specifically, whereas temporally broad excitation can lead to high-frequency oscillations in the ripple range, sparse pyramidal cell activity is only obtained with pulse-like external CA3 excitation. Further simulations indicate that such short pulses could originate from dendritic spikes in the apical or basal dendrites of CA1 pyramidal cells, which are triggered by coincident spike arrivals from hippocampal region CA3. Finally we show that replay of sequences by pyramidal neurons and ripple oscillations can arise intrinsically in CA1 due to structured connectivity that gives rise to alternating excitatory pulse and inhibitory gap coding; the latter implies phases of silence in specific basket cell groups and selective disinhibition of groups of pyramidal neurons. This general mechanism for sequence generation leads to sparse pyramidal cell and dense basket cell spiking, does not rely on synfire chain-like feedforward excitation and may be relevant for other brain regions as well.

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Section: Introductionsupporting

confidence: 67%

High-frequency oscillations and replay in a two-population model of hippocampal region CA1

Braun

Memmesheimer

2021

Preprint

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“…Unlike place cells observed in mammals, hippocampal activity reported in non-mammals is neither confined in space nor stable over time (14)(15)(16)(17)(18). In addition, nonmammalian SWRs have only been found outside of the hippocampus (19)(20)(21)(22).…”

mentioning

confidence: 97%

“…It is unknown whether these events originate in the hippocampus itself. In fact, SWRs have been reported in other brain regions of birds and reptiles (19)(20)(21). Regardless of their origin, it is unclear why hippocampal SWRs are experimentally detectable in birds.…”

mentioning

confidence: 99%

Neural representations of space in the hippocampus of a food-caching bird

Payne

Lynch

Aronov

2021

Science

116

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Spatial memory in vertebrates requires brain regions homologous to the mammalian hippocampus. Between vertebrate clades, however, these regions are anatomically distinct and appear to produce different spatial patterns of neural activity. We asked whether hippocampal activity is fundamentally different even between distant vertebrates that share a strong dependence on spatial memory. We studied tufted titmice, food-caching birds capable of remembering many concealed food locations. We found mammalian-like neural activity in the titmouse hippocampus, including sharp-wave ripples and anatomically organized place cells. In a non–food-caching bird species, spatial firing was less informative and was exhibited by fewer neurons. These findings suggest that hippocampal circuit mechanisms are similar between birds and mammals, but that the resulting patterns of activity may vary quantitatively with species-specific ethological needs.

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“…Such evidence suggests that the synaptic weights of the vast majority of cells in the immediate network vicinity are likely modulated by SWRs (Buzsáki, 2015;Norimoto et al, 2018), indicating that a given awake SWR may simultaneously serve a dual cognitive function of consolidating and for example, retrieving information (see Joo & Frank, 2018), or even consolidating and providing a non-cognitive function (Tingley, McClain, Kaya, Carpenter & Buzsáki, 2021). Importantly, similar SWR-like high frequency oscillations are also observed in other regions of the mammalian brain, during sleep in the claustrum homolog of reptiles and the hippocampal homolog in birds (Buzsáki, 2015;Norimoto et al, 2020;Payne et al, 2021;Yeganegi, Luksch & Ondracek, 2019).…”

Section: Cognitive Functions Of Sharp-wave Ripplesmentioning

confidence: 99%