scholarly journals Causal relations between cortical network oscillations and breathing frequency

2020 ◽  
Author(s):  
Adriano BL Tort ◽  
Maximilian Hammer ◽  
Jiaojiao Zhang ◽  
Jurij Brankačk ◽  
Andreas Draguhn

AbstractNasal breathing generates a rhythmic signal which entrains cortical network oscillations in widespread brain regions on a cycle-to-cycle time scale. It is unknown, however, how respiration and neuronal network activity interact on a larger time scale: are breathing frequency and typical neuronal oscillation patterns correlated? Is there any directionality or causal relationship? To address these questions, we recorded field potentials from the posterior parietal cortex of mice together with respiration during REM sleep. In this state, the parietal cortex exhibits prominent theta and gamma oscillations while behavioral activity is minimal, reducing confounding signals. We found that the instantaneous breathing rate strongly correlates with the instantaneous frequency and amplitude of both theta and gamma oscillations. Granger causality analysis revealed specific directionalities for different rhythms: changes in theta activity precede and cause changes in breathing rate, suggesting control of breathing frequency by the functional state of the brain. On the other hand, the instantaneous breathing rate Granger-causes changes in gamma oscillations, suggesting that gamma is influenced by a peripheral reafference signal. These findings show that breathing causally relates to different patterns of rhythmic brain activity, revealing new and complex interactions between elementary physiological functions and neuronal information processing.Significance StatementThe study of the interactions between respiration and brain activity has been focused on phase-entrainment relations, in which cortical networks oscillate phase-locked to breathing cycles. Here we discovered new and much broader interactions which link respiration rate (frequency) to different patterns of oscillatory brain activity. Specifically, we show that the instantaneous breathing rate strongly correlates with the instantaneous frequency and amplitude of theta and gamma oscillations, two major network patterns associated with cognitive functions. Interestingly, causality analyses reveal that changes in breathing rate follow theta, suggesting a central drive, while in contrast, gamma activity follows changes in breathing rate, suggesting the role of a reafferent signal. Our results reveal new mechanisms by which nasal breathing patterns may influence brain functions.

2020 ◽  
Author(s):  
Maximilian Hammer ◽  
Chrysovalandis Schwale ◽  
Jurij Brankačk ◽  
Andreas Draguhn ◽  
Adriano BL Tort

AbstractTemporal coupling between theta and gamma oscillations is a hallmark activity pattern of several cortical networks and becomes especially prominent during REM sleep. In a parallel approach, nasal breathing has been recently shown to generate phase-entrained network oscillations which also modulate gamma. Both slow rhythms (theta and respiration-entrained oscillations) have been suggested to aid large-scale integration but they differ in frequency, display low coherence, and modulate different gamma sub-bands. Respiration and theta are therefore believed to be largely independent. In the present work, however, we report an unexpected but robust relation between theta-gamma coupling and respiration in mice. Interestingly, this relation takes place not through the phase of individual respiration cycles, but through respiration rate: the strength of theta-gamma coupling exhibits an inverted V-shaped dependence on breathing rate, leading to maximal coupling at breathing frequencies of 4-6 Hz. Noteworthy, when subdividing sleep epochs into phasic and tonic REM patterns, we find that breathing differentially relates to theta-gamma coupling in each state, providing new evidence for their physiological distinctiveness. Altogether, our results reveal that breathing correlates with brain activity not only through phase-entrainment but also through rate-dependent relations with theta-gamma coupling. Thus, the link between respiration and other patterns of cortical network activity is more complex than previously assumed.


SLEEP ◽  
2021 ◽  
Author(s):  
Maximilian Hammer ◽  
Chrysovalandis Schwale ◽  
Jurij Brankačk ◽  
Andreas Draguhn ◽  
Adriano B L Tort

Abstract Temporal coupling between theta and gamma oscillations is a hallmark activity pattern of several cortical networks and becomes especially prominent during REM sleep. In a parallel approach, nasal breathing has been recently shown to generate phase-entrained network oscillations which also modulate gamma. Both slow rhythms (theta and respiration-entrained oscillations) have been suggested to aid large-scale integration but they differ in frequency, display low coherence, and modulate different gamma sub-bands. Respiration and theta are therefore believed to be largely independent. In the present work, however, we report an unexpected but robust relation between theta-gamma coupling and respiration in mice. Interestingly, this relation takes place not through the phase of individual respiration cycles, but through respiration rate: the strength of theta-gamma coupling exhibits an inverted V-shaped dependence on breathing rate, leading to maximal coupling at breathing frequencies of 4-6 Hz. Noteworthy, when subdividing sleep epochs into phasic and tonic REM patterns, we find that breathing differentially relates to theta-gamma coupling in each state, providing new evidence for their physiological distinctiveness. Altogether, our results reveal that breathing correlates with brain activity not only through phase-entrainment but also through rate-dependent relations with theta-gamma coupling. Thus, the link between respiration and other patterns of cortical network activity is more complex than previously assumed.


2021 ◽  
pp. JN-RM-3067-20
Author(s):  
Adriano BL Tort ◽  
Maximilian Hammer ◽  
Jiaojiao Zhang ◽  
Jurij Brankačk ◽  
Andreas Draguhn

1982 ◽  
Vol 96 (1) ◽  
pp. 53-67 ◽  
Author(s):  
JEFFREY B. GRAHAM ◽  
TROY A. BAIRD

In response to progressive aquatic hypoxia, the armoured loricariid catfishes Ancistrus chagresi and Hypostomus plecostomus become facultative air-breathers and utilize their stomachs as accessory air-breathing organs. Hypostomus initiates air breathing at a higher aquatic O2 tension (Pw, Ow, O2) than does Ancistrus (60 v. 33 mmHg). Once begun, the air-breathing frequencies of both species increase with decreasing Pw, Ow, O2; the frequency of Ancistrus, however, is greater than and increases more with hypoxia than does that of Hypostomus, which appears to be a more efficient air breather. Hypoxia acclimation reduces the air-breathing rate of both species. A larger rate reduction occurs in Ancistrus, which, however, continues to require more frequent breaths than Hypostomus. Hypoxia acclimation does not affect the air-breathing threshold of either species, suggesting that external O2 receptors initiate facultative air breathing. In progressive aquatic hypercapnia Ancistrus has a lower air-breathing CO2 threshold (8.7 mmHg) than Hypostomus (12.8 mmHg). However, in some tests, individual fish of both species did not initiate air breathing even at Pw, COw, CO2 as high as 21 mmHg. Also, air breathing evoked by hypercapnia was short-lived; both species quickly compensated for this gas and resumed exclusively aquatic respiration within a few hours of exposure. Thus, CO2 is not an important regulator of air breathing in these species. Between 25 and 35 °C, the Pw, Ow, O2 air breathing threshold of Ancistrus is temperature-independent, but air-breathing frequency increases with temperature. Ancistrus and Hypostomus do not breathe air in normoxic (air-saturated) water; their air-breathing responses are evoked by environmental hypoxia. This is fundamentally different from other fish species that breathe air in normoxia in order to meet heightened metabolic demands. Also, the facultative air-breathing adaptations of Ancistrus and Hypostomus differ in scope and magnitude from those utilized by species that breathe air in nor-moxia and adapt to hypoxia by increasing air-breathing rate.


2021 ◽  
Author(s):  
Ye Li ◽  
William Bosking ◽  
Michael S Beauchamp ◽  
Sameer A Sheth ◽  
Daniel Yoshor ◽  
...  

Narrowband gamma oscillations (NBG: ~20-60Hz) in visual cortex reflect rhythmic fluctuations in population activity generated by underlying circuits tuned for stimulus location, orientation, and color. Consequently, the amplitude and frequency of induced NBG activity is highly sensitive to these stimulus features. For example, in the non-human primate, NBG displays biases in orientation and color tuning at the population level. Such biases may relate to recent reports describing the large-scale organization of single-cell orientation and color tuning in visual cortex, thus providing a potential bridge between measurements made at different scales. Similar biases in NBG population tuning have been predicted to exist in the human visual cortex, but this has yet to be fully examined. Using intracranial recordings from human visual cortex, we investigated the tuning of NBG to orientation and color, both independently and in conjunction. NBG was shown to display a cardinal orientation bias (horizontal) and also an end- and mid-spectral color bias (red/blue and green). When jointly probed, the cardinal bias for orientation was attenuated and an end-spectral preference for red and blue predominated. These data both elaborate on the close, yet complex, link between the population dynamics driving NBG oscillations and known feature selectivity biases in visual cortex, adding to a growing set of stimulus dependencies associated with the genesis of NBG. Together, these two factors may provide a fruitful testing ground for examining multi-scale models of brain activity, and impose new constraints on the functional significance of the visual gamma rhythm.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Lu Zhang ◽  
John Lee ◽  
Christopher Rozell ◽  
Annabelle C Singer

Oscillatory brain activity reflects different internal brain states including neurons’ excitatory state and synchrony among neurons. However, characterizing these states is complicated by the fact that different oscillations are often coupled, such as gamma oscillations nested in theta in the hippocampus, and changes in coupling are thought to reflect distinct states. Here, we describe a new method to separate single oscillatory cycles into distinct states based on frequency and phase coupling. Using this method, we identified four theta-gamma coupling states in rat hippocampal CA1. These states differed in abundance across behaviors, phase synchrony with other hippocampal subregions, and neural coding properties suggesting that these states are functionally distinct. We captured cycle-to-cycle changes in oscillatory coupling states and found frequent switching between theta-gamma states showing that the hippocampus rapidly shifts between different functional states. This method provides a new approach to investigate oscillatory brain dynamics broadly.


2007 ◽  
Vol 98 (1) ◽  
pp. 96-104 ◽  
Author(s):  
Jay Spampanato ◽  
Istvan Mody

Network activity in the 200- to 600-Hz range termed high-frequency oscillations (HFOs) has been detected in epileptic tissue from both humans and rodents and may underlie the mechanism of epileptogenesis in experimental rodent models. Slower network oscillations including theta and gamma oscillations as well as ripples are generated by the complex spike timing and interactions between interneurons and pyramidal cells of the hippocampus. We determined the activity of CA3 pyramidal cells, stratum oriens lacunosum-moleculare (O-LM) and s. radiatum lacunosum-moleculare (R-LM) interneurons during HFO in the in vitro low-Mg2+ model of epileptiform activity in GIN mice. In these animals, interneurons can be identified prior to cell-attached recordings by the expression of green-fluorescent protein (GFP). Simultaneous local field potential recordings from s. pyramidale and on-cell recordings of individual interneurons and principal cells revealed three primary firing behaviors of the active cells: 36% of O-LM interneurons and 60% of pyramidal cells fired action potentials at high frequencies during the HFO. R-LM interneurons were biphasic in that they fired at high frequency at the beginning of the HFO but stopped firing before its end. When considering only the highest frequency component of the oscillations most pyramidal cells fired on the rising phase of the oscillation. These data provide evidence for functional distinction during HFOs within otherwise homogeneous groups of O-LM interneurons and pyramidal cells.


2016 ◽  
Vol 113 (46) ◽  
pp. 13251-13256 ◽  
Author(s):  
Svenja Brodt ◽  
Dorothee Pöhlchen ◽  
Virginia L. Flanagin ◽  
Stefan Glasauer ◽  
Steffen Gais ◽  
...  

Previous evidence indicates that the brain stores memory in two complementary systems, allowing both rapid plasticity and stable representations at different sites. For memory to be established in a long-lasting neocortical store, many learning repetitions are considered necessary after initial encoding into hippocampal circuits. To elucidate the dynamics of hippocampal and neocortical contributions to the early phases of memory formation, we closely followed changes in human functional brain activity while volunteers navigated through two different, initially unknown virtual environments. In one condition, they were able to encode new information continuously about the spatial layout of the maze. In the control condition, no information could be learned because the layout changed constantly. Our results show that the posterior parietal cortex (PPC) encodes memories for spatial locations rapidly, beginning already with the first visit to a location and steadily increasing activity with each additional encounter. Hippocampal activity and connectivity between the PPC and hippocampus, on the other hand, are strongest during initial encoding, and both decline with additional encounters. Importantly, stronger PPC activity related to higher memory-based performance. Compared with the nonlearnable control condition, PPC activity in the learned environment remained elevated after a 24-h interval, indicating a stable change. Our findings reflect the rapid creation of a memory representation in the PPC, which belongs to a recently proposed parietal memory network. The emerging parietal representation is specific for individual episodes of experience, predicts behavior, and remains stable over offline periods, and must therefore hold a mnemonic function.


2003 ◽  
Vol 15 (7) ◽  
pp. 1002-1018 ◽  
Author(s):  
Jeffrey M. Zacks ◽  
Jean M. Vettel ◽  
Pascale Michelon

Human spatial reasoning may depend in part on two dissociable types of mental image transformations: objectbased transformations, in which an object is imagined to move in space relative to the viewer and the environment, and perspective transformations, in which the viewer imagines the scene from a different vantage point. This study measured local brain activity with event-related fMRI while participants were instructed to either imagine an array of objects rotating (an object-based transformation) or imagine themselves rotating around the array (a perspective transformation). Object-based transformations led to selective increases in right parietal cortex and decreases in left parietal cortex, whereas perspective transformations led to selective increases in left temporal cortex. These results argue against the view that mental image transformations are performed by a unitary neural processing system, and they suggest that different overlapping systems are engaged for different image transformations.


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