Hippocampal strata theta oscillations change their frequency and coupling during spatial learning

Hernández-Pérez, J. Jesús; Gutiérrez-Guzmán, Blanca Erika; Olvera‐Cortés, María Esther

doi:10.1016/j.neuroscience.2016.09.003

Cited by 25 publications

(33 citation statements)

References 92 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…regions (Florian and Roullet, 2004), in which Gpr158 is expressed (Condomitti et al, 2018;Khrimian et al, 2017). Theta frequency coupling between CA3 and CA1 is enhanced during MWM learning, when there is a clear improvement in task performance (Hernández-Pérez et al, 2016). The changes in CA1 morphology and excitability we report along with the changes in CA3 physiology (Condomitti et al, 2018) could alter such coupling, hence impacting learning in Gpr158 KO mice.…”

Section: Acquisition Of a Safety Memory And Spatial Memory Are Affectmentioning

confidence: 74%

Gpr158 deficiency impacts hippocampal CA1 neuronal excitability, dendritic architecture, and affects spatial learning

Çetereisi

Kramvis

Gebuis

et al. 2018

Preprint

View full text Add to dashboard Cite

G-protein-coupled receptor 158 (Gpr158) is highly expressed in striatum, hippocampus and prefrontal cortex.It gained attention as it was implicated in physiological responses to stress and depression. Recently, Gpr158has been shown to act as a pathway-specific synaptic organizer in the hippocampus, required for proper mossy fiber-CA3 neurocircuitry establishment, structure, and function. Although rodent Gpr158 expression is highest in CA3, considerable expression occurs in CA1 especially after the first postnatal month. Here, we combined hippocampal-dependent behavioral paradigms with subsequent electrophysiological and morphological analyses from the same group of mice to assess the effects of Gpr158 deficiency on CA1 physiology and function. We demonstrate deficits in spatial memory acquisition and retrieval in the Morris water maze paradigm, along with deficits in the acquisition of extinction memory in the passive avoidance test in Gpr158 KO mice. Electrophysiological recordings from CA1 pyramidal neurons revealed normal basal excitatory and inhibitory synaptic transmission, however, Schaffer collateral stimulation yielded dramatically reduced post-synaptic currents. Interestingly, intrinsic excitability of CA1 pyramidals was found increased, potentially acting as a compensatory mechanism to the reductions in Schaffer collateral-mediated drive. Both ex vivo and in vitro, neurons deficient for Gpr158 exhibited robust reductions in dendritic architecture and complexity, i.e., reduced length, surface, bifurcations, and branching. This effect was localized in the apical but not basal compartment of adult CA1 pyramidals, indicative of pathway-specific alterations. A significant positive correlation between spatial memory acquisition and extent of complexity of CA1 pyramidals was found. Taken together, we provide first evidence of significant disruptions in hippocampal CA1 neuronal dendritic architecture and physiology, driven by Gpr158 deficiency. Importantly, the hippocampal neuronal morphology deficits appear to support the impairments in spatial memory acquisition observed in Gpr158 KO mice.Çetereisi & Kramvis et al. Gpr158 impacts hippocampal CA1 dendritic architecture and spatial learning

show abstract

Section: Acquisition Of a Safety Memory And Spatial Memory Are Affectmentioning

confidence: 74%

Gpr158 deficiency impacts hippocampal CA1 neuronal excitability, dendritic architecture, and affects spatial learning

Çetereisi

Kramvis

Gebuis

et al. 2018

Preprint

View full text Add to dashboard Cite

show abstract

“…Although swimming is natural and a normal mode of locomotion in rodents, past studies have indicated a lack of theta-speed relationship in swimming rats (Whishaw and Vanderwolf, 1973), presumably due to a disruption of proprioception associated with conventional ambulation on land. A more detailed study on hippocampal theta frequency and swimming speed have revealed an unreliable relationship at best (Hernandez-Perez et al, 2016) – although the use of conventional FFT-based spectral analysis in this study may have yielded less accurate estimates due to the non-stationary nature of brain field potentials and the time-frequency trade-off (Young and Eggermont, 2009).…”

Section: Introductionmentioning

confidence: 83%

“…Hippocampal theta has many behavioural correlates (Vanderwolf, 1969; Buzsaki, 2005; Young, 2011; Korotkova et al, 2018), the most salient among them is its linear scaling with the speed of ongoing locomotion, in both frequency (McFarland et al, 1975; Slawinska and Kasicki, 1998; Jeewajee et al, 2008; Wells et al, 2013; Aghajan et al, 2017) and power (Rivas et al, 1996; Maurer et al, 2005; Watrous et al, 2011; Ahmed and Mehta, 2012). Despite various replications in independent laboratories, linear locomotion speed and hippocampal theta correlation can be highly variable between animals and recording sessions (Richard et al, 2013; Hernandez-Perez et al, 2016). It has been suggested that variability in the speed-theta correlations may be modulated by other functions that are dependent on theta oscillations, such as learning and memory (Montgomery et al, 2009; Richard et al, 2013; Schmidt et al, 2013; Belchior et al, 2014; Hernandez-Perez et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Despite various replications in independent laboratories, linear locomotion speed and hippocampal theta correlation can be highly variable between animals and recording sessions (Richard et al, 2013; Hernandez-Perez et al, 2016). It has been suggested that variability in the speed-theta correlations may be modulated by other functions that are dependent on theta oscillations, such as learning and memory (Montgomery et al, 2009; Richard et al, 2013; Schmidt et al, 2013; Belchior et al, 2014; Hernandez-Perez et al, 2016). Certainly, abolishing hippocampal theta oscillations do not result in the abolishment of movement, but is correlated to spatial learning deficits (Winson, 1978; McNaughton et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Speed modulation of hippocampal theta frequency and power predicts water maze learning

Young

Ruan

McNaughton

2020

Preprint

View full text Add to dashboard Cite

3Theta oscillations in the hippocampus have many behavioural correlates, with the 2 4 magnitude and vigour of ongoing movement being the most salient. Many consider 2 5 correlates of locomotion with hippocampal theta to be a confound in delineating theta 2 6 contributions to cognitive processes. But, theory and empirical experiments suggest 2 7 theta-movement relationships are important if spatial navigation is to support higher 2 8 cognitive processes. In the current study, we tested if variations in speed modulation 2 9 of hippocampal theta can predict spatial learning rates in the water maze. Using 3 0 multi-step regression, we find the magnitude and robustness of hippocampal theta 3 1 frequency versus speed scaling can predict water maze learning rates. Using 3 2 generalised linear models, we also demonstrate that speed and water maze learning 3 3 are the best predictors of hippocampal theta frequency and power. Theta oscillations 3 4recorded from the supramammillary area showed much weaker, or non-existent, 3 5 relationships, which supports the idea that hippocampal theta has specific roles in 3 6 speed representation and spatial learning. Our findings suggest movement-speed 3 7

show abstract

“…Theta is well understood both in terms of its underlying physiology and its potential function (for reviews, see Buzsáki, 2002;Dickson et al, 2000;Vinogradova, 1995). Functionally, theta is attributed with supporting navigation (Blair et al, 2007;Brandon et al, 2011;Burgess et al, 2007;Newman and Hasselmo, 2014;Onslow et al, 2014), mediating associational learning (Caplan et al, 2003;Hasselmo et al, 2002;Hernández-Pérez et al, 2015;2016;Honey et al, 2017;Muller et al, 2018;Norman et al, 2006;Patel et al, 2012), and pacing the relative timing of the distinct components of the entorhinal-hippocampal circuit (Mizuseki et al, 2009). These proposed functions are not mutually exclusive.…”

Section: Introductionmentioning

confidence: 99%

Medial entorhinal cortex activates in a traveling wave

Perez

Cooper²,

Newman³

2019

Preprint

View full text Add to dashboard Cite

Traveling waves of cortical activity are hypothesized to organize cortical information processing and support interregional communication. Yet, it remains unknown whether interacting areas exhibit the matched traveling waves necessary to support this hypothesized form of interaction.Here, we show that the strongly-interacting medial entorhinal cortex (MEC) and hippocampus exhibit matched traveling waves. We demonstrate that both the field potential and spiking in the MEC exhibit prominent 6-12 Hz 'theta' traveling waves matching those of the hippocampus. The theta phase shifts observed along the MEC were accounted for largely by variation in waveform asymmetry. From this, we hypothesize that that gradients in local physiology underlie both the generation of MEC traveling waves and the functional variations observed previously across the MEC.

show abstract

Hippocampal strata theta oscillations change their frequency and coupling during spatial learning

Cited by 25 publications

References 92 publications

Gpr158 deficiency impacts hippocampal CA1 neuronal excitability, dendritic architecture, and affects spatial learning

Gpr158 deficiency impacts hippocampal CA1 neuronal excitability, dendritic architecture, and affects spatial learning

Speed modulation of hippocampal theta frequency and power predicts water maze learning

Medial entorhinal cortex activates in a traveling wave

Contact Info

Product

Resources

About