Recurrent thalamo-cortical resonance

Last updated

Recurrent thalamo-cortical resonance or Thalamocortical oscillation is an observed phenomenon of oscillatory neural activity between the thalamus and various cortical regions of the brain. It is proposed by Rodolfo Llinas and others as a theory for the integration of sensory information into the whole of perception in the brain. [1] [2] Thalamocortical oscillation is proposed to be a mechanism of synchronization between different cortical regions of the brain, a process known as temporal binding. [3] This is possible through the existence of thalamocortical networks, groupings of thalamic and cortical cells that exhibit oscillatory properties.

Contents

Thalamocortical oscillation involves the synchronous firing of thalamic and cortical neurons at specific frequencies; in the thalamocortical system, the exact frequencies depend on current brain state and mental activity. Fast frequencies in the gamma range are associated with much of conscious thought and active cognition. The thalamus in this system acts as both the gate for sensory input to the cortex as well as the site for feedback from cortical pyramidal cells, implying a processing role in sensory perception in addition to its function in directing information flow. The state of the brain, whether it be conscious, in REM sleep, or non-rapid eye movement sleep, changes how sensory information is gated through the thalamus.

Thalamocortical network structure

Thalamocortical networks consist of neurons in both the thalamus and cortex. The thalamic neurons are typically one of three types: thalamocortical, with axons extending into the cortex, reticular, and thalamic interneurons. [4] Thalamocortical neurons (TC) vary significantly in size, which is correlated with the depth to which they project into the cortex. These cells are limited in their outputs and seem to only connect to the cortical layers and reticular thalamic neurons. Reticular neurons (RE), on the other hand, are highly interconnected and have their own intrinsic oscillatory properties. These neurons are capable of inhibiting thalamocortical activity via their direct connections to TCs. Corticothalamic neurons are the cortical neurons that TC neurons synapse on. These cells are glutaminergic excitatory cells that exhibit increasing activity as they become more depolarized. This activity is described as "bursting", firing in the gamma range at rates between 20 and 50 Hz.

Thalamic oscillation

EEG signal filtered to show only gamma wave brain activity. Eeg gamma.svg
EEG signal filtered to show only gamma wave brain activity.

The thalamocortical loop starts with oscillatory thalamic cells. These cells receive both sensory input from the body as well as input from feedback pathways in the brain. In a sense, these cells serve to integrate these multiple inputs by changing their inherent oscillatory properties in response to depolarization by these many different inputs. TC neurons exhibit gamma oscillation when depolarized to greater than −45 mV, [2] and the frequency of oscillation is related to the degree of depolarization. [5] This oscillation is caused by the activation of leaky P/Q-type calcium channels found in the dendrites of the cells. [5] Because of the leaky channel properties, spontaneous, inherent oscillation can also occur independent of any rhythmic input as well, [2] though the ramifications of this capability are not entirely known and may add nothing but background noise to the thalamocortical loop.

The cortex provides feedback to the thalamus through links to dendrites of these thalamocortical cells and serves as the source of constant thalamic oscillation. Oscillatory behavior depends on the conscious/unconscious state of the brain. During active thinking, electroencephalography reveals a strong appearance of gamma range oscillation from around 20–50 Hz. [2] [6]

Thalamocortical circuits

Thalamic cells synapse on apical dendrites of pyramidal cells in the cortex. These pyramidal cells reciprocally synapse back on thalamic neurons. Each loop is self-contained and modulated by sensory input. Inhibitory interneurons both in the cortex and the reticular nucleus of the thalamus regulate circuit activity.

Inputs to thalamocortical system

Thalamocortical circuit diagram depicting both specific/sensory and non-specific intralaminar thalamocortical systems. Tc circuit.png
Thalamocortical circuit diagram depicting both specific/sensory and non-specific intralaminar thalamocortical systems.

The thalamus gates information into thalamocortical loops based on the source of the signal. There are two major sources for TC input: sensory perception and information about the current mental state. Cortical structures of external events or sensory data are referred to as specific inputs and enter into the ventrobasal thalamus at the "specific" thalamic nuclei. [2] These neurons project to layer IV of the cortex. Similarly, nonspecific inputs provide context from internal state of the brain and enter into intralaminar "non-specific" nuclei in the centrolateral thalamus with axons in layers I and VI. [2] Both types of TC neurons synapse on the pyramidal cortical cells which are thought to integrate the signals. In this way, outside sensory information is introduced into the current context of cognition.

Resonant columns

Studies involving manipulation of slices of visual cortex have shown that thalamocortical resonance from stimulated TCs induces the formation of coherent regions of similar electrical activity through vertical layers of the cortex. [2] In essence this means that groupings of activated cortical cells form from the activation of these thalamic cells. These regions are columnar and are physically separated from adjacent resonance columns by areas of inhibited cortex between them. It is not known what the exact function of these columns is, although their formation occurs only when the cortical white matter afferents are stimulated at the gamma frequency range, implying an association with task-focused thought. The regions of inactive cortex that form between cortical columns were determined to be actively inhibited; administration of a GABA A blocker stops columnar development.

Temporal binding

Thalamocortical resonance is thought to be a potential explanation for coherence of perception in the brain. Temporal coincidence could occur through this mechanism by the integration of both specific and non-specific thalamic nuclei at the pyramidal cortical cell, as they both synapse on its apical dendrites. [6] Feedback from the cortical cell back to the thalamic nuclei then relays the integrated signal. As there are numerous thalamocortical loops throughout the cortex, this process takes place simultaneously across many different regions of the brain during conscious perception. It is this ability to support large-scale synchronized events between remote brain regions that may provide for coherent perception. Altogether, the specific, ventrobasal neurons in the thalamus serve to introduce sensory input to a self-sustained feedback loop that is sustained by the non-specific, centrolateral TCs relaying information about the current cognitive state of the brain.

Relation to brain activity

The human visual pathway. The lateral geniculate nucleus, a region of the thalamus, exhibits thalamocortical oscillation with the visual cortex. Gray722.png
The human visual pathway. The lateral geniculate nucleus, a region of the thalamus, exhibits thalamocortical oscillation with the visual cortex.

Thalamocortical oscillation is thought to be responsible for the synchronization of neural activity between different regions of the cortex and is associated with the appearance of specific mental states depending on the frequency range of the most prominent oscillatory activity, gamma most associated with conscious, selective concentration on tasks, [8] learning (perceptual and associative), [9] and short-term memory. [10] Magnetoencephalography (MEG) has been used to show that during conscious perception, gamma-band frequency electrical activity and thalamocortical resonance prominently occurs in the human brain. [2] Absence of these gamma-band patterns correlates with nonconscious states and is characterized by the presence of lower-frequency oscillations instead.

Vision

The lateral geniculate nucleus, known as the major relay center from the sensory neurons in the eyes to the visual cortex, is found in the thalamus and has thalamocortical oscillatory properties, [7] forming a feedback loop between the thalamus and the visual cortex. Sensory input can be seen to modulate the oscillatory patterns of thalamocortical activity while awake. In the case of vision, stimulation from light sources can be seen to cause direct changes in the amplitude of the thalamocortical oscillations as measured by EEG. [11]

Sleep

Gamma wave thalamocortical oscillation is prominent during REM sleep, similar to the awakened, active brain. [2] Contrary to the conscious state, however, it appears that sensory input may be blocked or gated from interfering with the intrinsic activity of the brain during REM. Measures of bulk electrical signalling in the brain by MEG show no impact of auditory stimuli on the gamma wave patterns; measurements on conscious subjects show a distinct modulation due to the auditory input. In this way, the thalamocortical system acts to gate the brain from external stimuli during REM.

Non-rapid eye movement (NREM) sleep differs from REM in that gamma activity is no longer prominent, stepping aside for lower frequency oscillations. While electrical activity at gamma frequencies can occasionally be detected in NREM, it is infrequent and comes in bursts. [5] The exact purpose of its appearance in NREM is not understood. In NREM sleep, thalamocortical oscillatory activity is still present, but the overall frequencies range from the slow (<1 Hz), to the delta (1–4 Hz), and theta (4–7 Hz) range. [12] Synchronized theta oscillation has additionally been observed in the hippocampus during NREM. [12]

Alpha oscillations and attention

Gamma-range oscillations are not the only rhythms associated with conscious thought and activity. Thalamocortical alpha frequency oscillations have been noted in the human occipital-parietal cortex. This activity could be originated by the pyramidal neurons in layer IV. [3] It has been shown that alpha rhythms seem to be related to the focus of one's attention: external focus on visual tasks diminishes alpha activity while internal focus as in heavy working memory tasks show an increase in alpha magnitudes. [3] This is contrary to gamma wave oscillatory frequencies which emerge in selective focus tasks.

Thalamocortical dysrhythmia

Thalamocortical dysrhythmia (TCD) is a proposed explanation for certain cognitive disorders. It occurs upon the disruption of normal gamma-band electrical activity between the cortex and thalamic neurons during awakened, conscious states. [13] This disorder is associated with diseases and conditions such as neuropathic pain, tinnitus, and Parkinson's disease [14] and is characterized by the presence of unusually low-frequency resonance in the thalamocortical system. TCD is associated with disruption of many brain functions including cognition, sensory perception, and motor control and occurs when thalamocortical neurons become inappropriately hyperpolarized, allowing T-type calcium channels to activate and the oscillatory properties of the thalamocortical neurons to change. [13] A repeated burst of action potentials occurs at lower frequencies in the 4–10 Hz range. These bursts can be sustained by inhibition from the thalamic reticular nucleus and may cause an activation of cortical regions that are normally inhibited by gamma-band activity during resonance column formation. While the effect of the deviation from normal patterns of gamma oscillatory activity during conscious perception is not entirely settled, it is proposed that the phenomenon can be used to explain chronic pain in cases where there is no specific peripheral nerve damage.

See also

Related Research Articles

<span class="mw-page-title-main">Cerebral cortex</span> Outer layer of the cerebrum of the mammalian brain

The cerebral cortex, also known as the cerebral mantle, is the outer layer of neural tissue of the cerebrum of the brain in humans and other mammals. It is the largest site of neural integration in the central nervous system, and plays a key role in attention, perception, awareness, thought, memory, language, and consciousness. The cerebral cortex is the part of the brain responsible for cognition.

<span class="mw-page-title-main">Thalamus</span> Structure within the brain

The thalamus is a large mass of gray matter on the lateral walls of the third ventricle forming the dorsal part of the diencephalon. Nerve fibers project out of the thalamus to the cerebral cortex in all directions, known as the thalamocortical radiations, allowing hub-like exchanges of information. It has several functions, such as the relaying of sensory and motor signals to the cerebral cortex and the regulation of consciousness, sleep, and alertness.

<span class="mw-page-title-main">Trigeminal nerve</span> Cranial nerve responsible for the faces senses and motor functions

In neuroanatomy, the trigeminal nerve (lit. triplet nerve), also known as the fifth cranial nerve, cranial nerve V, or simply CN V, is a cranial nerve responsible for sensation in the face and motor functions such as biting and chewing; it is the most complex of the cranial nerves. Its name (trigeminal, from Latin tri- 'three' and -geminus 'twin') derives from each of the two nerves (one on each side of the pons) having three major branches: the ophthalmic nerve (V1), the maxillary nerve (V2), and the mandibular nerve (V3). The ophthalmic and maxillary nerves are purely sensory, whereas the mandibular nerve supplies motor as well as sensory (or "cutaneous") functions. Adding to the complexity of this nerve is that autonomic nerve fibers as well as special sensory fibers (taste) are contained within it.

<span class="mw-page-title-main">Rodolfo Llinás</span> Colombian neuroscientist (born 1934)

Rodolfo Llinás Riascos is a Colombian and American neuroscientist. He is currently the Thomas and Suzanne Murphy Professor of Neuroscience and Chairman Emeritus of the Department of Physiology & Neuroscience at the NYU School of Medicine. Llinás has published over 800 scientific articles.

<span class="mw-page-title-main">Reticular formation</span> Spinal trigeminal nucleus

The reticular formation is a set of interconnected nuclei in the brainstem that spans from the lower end of the medulla oblongata to the upper end of the midbrain. The neurons of the reticular formation make up a complex set of neural networks in the core of the brainstem. It is not anatomically well defined, because it includes neurons located in different parts of the brain.

A gamma wave or gamma rhythm is a pattern of neural oscillation in humans with a frequency between 30 and 100 Hz, the 40 Hz point being of particular interest. Gamma rhythms are correlated with large-scale brain network activity and cognitive phenomena such as working memory, attention, and perceptual grouping, and can be increased in amplitude via meditation or neurostimulation. Altered gamma activity has been observed in many mood and cognitive disorders such as Alzheimer's disease, epilepsy, and schizophrenia.

<span class="mw-page-title-main">Thalamic reticular nucleus</span>

The thalamic reticular nucleus is part of the ventral thalamus that forms a capsule around the thalamus laterally. However, recent evidence from mice and fish question this statement and define it as a dorsal thalamic structure. It is separated from the thalamus by the external medullary lamina. Reticular cells are GABAergic, and have discoid dendritic arbors in the plane of the nucleus.

Sleep spindles are bursts of neural oscillatory activity that are generated by interplay of the thalamic reticular nucleus (TRN) and other thalamic nuclei during stage 2 NREM sleep in a frequency range of ~11 to 16 Hz with a duration of 0.5 seconds or greater. After generation as an interaction of the TRN neurons and thalamocortical cells, spindles are sustained and relayed to the cortex by thalamo-thalamic and thalamo-cortical feedback loops regulated by both GABAergic and NMDA-receptor mediated glutamatergic neurotransmission. Sleep spindles have been reported for all tested mammalian species. Considering animals in which sleep-spindles were studied extensively, they appear to have a conserved main frequency of roughly 9–16 Hz. Only in humans, rats and dogs is a difference in the intrinsic frequency of frontal and posterior spindles confirmed, however.

<span class="mw-page-title-main">Thalamocortical radiations</span> Neural pathways between the thalamus and cerebral cortex

In neuroanatomy, thalamocortical radiations, also known as thalamocortical fibers, are the efferent fibers that project from the thalamus to distinct areas of the cerebral cortex. They form fiber bundles that emerge from the lateral surface of the thalamus.

Brainwave entrainment, also referred to as brainwave synchronization or neural entrainment, refers to the observation that brainwaves will naturally synchronize to the rhythm of periodic external stimuli, such as flickering lights, speech, music, or tactile stimuli.

<span class="mw-page-title-main">Neural oscillation</span> Brainwaves, repetitive patterns of neural activity in the central nervous system

Neural oscillations, or brainwaves, are rhythmic or repetitive patterns of neural activity in the central nervous system. Neural tissue can generate oscillatory activity in many ways, driven either by mechanisms within individual neurons or by interactions between neurons. In individual neurons, oscillations can appear either as oscillations in membrane potential or as rhythmic patterns of action potentials, which then produce oscillatory activation of post-synaptic neurons. At the level of neural ensembles, synchronized activity of large numbers of neurons can give rise to macroscopic oscillations, which can be observed in an electroencephalogram. Oscillatory activity in groups of neurons generally arises from feedback connections between the neurons that result in the synchronization of their firing patterns. The interaction between neurons can give rise to oscillations at a different frequency than the firing frequency of individual neurons. A well-known example of macroscopic neural oscillations is alpha activity.

<span class="mw-page-title-main">Neural binding</span>

Neural binding is the neuroscientific aspect of what is commonly known as the binding problem: the interdisciplinary difficulty of creating a comprehensive and verifiable model for the unity of consciousness. "Binding" refers to the integration of highly diverse neural information in the forming of one's cohesive experience. The neural binding hypothesis states that neural signals are paired through synchronized oscillations of neuronal activity that combine and recombine to allow for a wide variety of responses to context-dependent stimuli. These dynamic neural networks are thought to account for the flexibility and nuanced response of the brain to various situations. The coupling of these networks is transient, on the order of milliseconds, and allows for rapid activity.

The zona incerta (ZI) is a horizontally elongated small nucleus that separates the larger subthalamic nucleus from the thalamus. Its connections project extensively over the brain from the cerebral cortex down into the spinal cord.

Thalamocortical dysrhythmia (TCD) is a theoretical framework in which neuroscientists try to explain the positive and negative symptoms induced by neuropsychiatric disorders like Parkinson's Disease, neurogenic pain, tinnitus, visual snow syndrome, schizophrenia, obsessive–compulsive disorder, depressive disorder and epilepsy. In TCD, normal thalamocortical resonance is disrupted by changes in the behaviour of neurons in the thalamus.
TCD can be treated with neurosurgical methods like the central lateral thalamotomy, which due to its invasiveness is only used on patients that have proven resistant to conventional therapies.

<span class="mw-page-title-main">Subthreshold membrane potential oscillations</span>

Subthreshold membrane potential oscillations are membrane oscillations that do not directly trigger an action potential since they do not reach the necessary threshold for firing. However, they may facilitate sensory signal processing.

<span class="mw-page-title-main">Spike-and-wave</span>

Spike-and-wave is a pattern of the electroencephalogram (EEG) typically observed during epileptic seizures. A spike-and-wave discharge is a regular, symmetrical, generalized EEG pattern seen particularly during absence epilepsy, also known as ‘petit mal’ epilepsy. The basic mechanisms underlying these patterns are complex and involve part of the cerebral cortex, the thalamocortical network, and intrinsic neuronal mechanisms.

The trisynaptic circuit or trisynaptic loop is a relay of synaptic transmission in the hippocampus. The trisynaptic circuit is a neural circuit in the hippocampus, which is made up of three major cell groups: granule cells in the dentate gyrus, pyramidal neurons in CA3, and pyramidal neurons in CA1. The hippocampal relay involves 3 main regions within the hippocampus which are classified according to their cell type and projection fibers. The first projection of the hippocampus occurs between the entorhinal cortex (EC) and the dentate gyrus (DG). The entorhinal cortex transmits its signals from the parahippocampal gyrus to the dentate gyrus via granule cell fibers known collectively as the perforant path. The dentate gyrus then synapses on pyramidal cells in CA3 via mossy cell fibers. CA3 then fires to CA1 via Schaffer collaterals which synapse in the subiculum and are carried out through the fornix. Collectively the dentate gyrus, CA1 and CA3 of the hippocampus compose the trisynaptic loop.

<span class="mw-page-title-main">Neuroscience of sleep</span> Study of the neuroscientific and physiological basis of the nature of sleep

The neuroscience of sleep is the study of the neuroscientific and physiological basis of the nature of sleep and its functions. Traditionally, sleep has been studied as part of psychology and medicine. The study of sleep from a neuroscience perspective grew to prominence with advances in technology and the proliferation of neuroscience research from the second half of the twentieth century.

The neuroscience of rhythm refers to the various forms of rhythm generated by the central nervous system (CNS). Nerve cells, also known as neurons in the human brain are capable of firing in specific patterns which cause oscillations. The brain possesses many different types of oscillators with different periods. Oscillators are simultaneously outputting frequencies from .02 Hz to 600 Hz. It is now well known that a computer is capable of running thousands of processes with just one high-frequency clock. Humans have many different clocks as a result of evolution. Prior organisms had no need for a fast-responding oscillator. This multi-clock system permits quick response to constantly changing sensory input while still maintaining the autonomic processes that sustain life. This method modulates and controls a great deal of bodily functions.

Sharp waves and ripples (SWRs) are oscillatory patterns produced by extremely synchronised activity of neurons in the mammalian hippocampus and neighbouring regions which occur spontaneously in idle waking states or during NREM sleep. They can be observed with a variety of imaging methods, such as EEG. They are composed of large amplitude sharp waves in local field potential and produced by tens of thousands of neurons firing together within 30–100 ms window. They are some of the most synchronous oscillations patterns in the brain, making them susceptible to pathological patterns such as epilepsy.They have been extensively characterised and described by György Buzsáki and have been shown to be involved in memory consolidation in NREM sleep and the replay of memories acquired during wakefulness.

References

  1. Rodolfo R. Llin's (2002). I of the vortex: from neurons to self . MIT Press. ISBN   978-0-262-62163-2.
  2. 1 2 3 4 5 6 7 8 9 Llinás R, Ribary U, Contreras D, Pedroarena C (November 1998). "The neuronal basis for consciousness". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 353 (1377): 1841–9. doi:10.1098/rstb.1998.0336. PMC   1692417 . PMID   9854256.
  3. 1 2 3 Bollimunta, Anil (2011). "Neuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations". The Journal of Neuroscience. 31 (13): 4935–4943. doi:10.1523/JNEUROSCI.5580-10.2011. PMC   3505610 . PMID   21451032.
  4. Steriade, M (2000). "Corticothalamic resonance, states of vigilance and mentation". Neuroscience. 101 (2): 243–276. doi:10.1016/s0306-4522(00)00353-5. PMID   11074149. S2CID   38571191.
  5. 1 2 3 Steriade, Mircea (1997). "Synchronized Activities of Coupled Oscillators in the Cerebral Cortex and Thalamus at Different Levels of Vigilance". Cerebral Cortex. 7 (6): 583–604. doi: 10.1093/cercor/7.6.583 . PMID   9276182.
  6. 1 2 Llinas, Rodolfo (2002). "Temporal binding via coincidence detection of specific and nonspecific thalamocortical inputs: A voltage-dependent dye-imaging study in mouse brain slices". PNAS. 99 (1): 449–454. doi: 10.1073/pnas.012604899 . PMC   117580 . PMID   11773628.
  7. 1 2 Hughes, Stuart (2004). "Synchronized Oscillations at Alpha and Theta Frequencies in the Lateral Geniculate Nucleus". Neuron. 42 (2): 253–268. doi: 10.1016/s0896-6273(04)00191-6 . PMID   15091341.
  8. Tiitinen, H (1993). "Selective attention enhances the auditory 40-Hz transient response in humans". Nature. 364 (6432): 59–60. Bibcode:1993Natur.364...59T. doi:10.1038/364059a0. PMID   8316297. S2CID   4322755.
  9. Miltner, W (1999). "Coherence of gamma-band EEG activity as a basis for associative learning". Nature. 397 (6718): 434–436. Bibcode:1999Natur.397..434M. doi:10.1038/17126. PMID   9989409. S2CID   4379472.
  10. Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J (June 1998). "Induced gamma-band activity during the delay of a visual short-term memory task in humans". The Journal of Neuroscience. 18 (11): 4244–54. doi: 10.1523/JNEUROSCI.18-11-04244.1998 . PMC   6792803 . PMID   9592102.
  11. Rodriguez, Rosa (2004). "Short- and Long-Term Effects of Cholinergic Modulation on Gamma Oscillations and Response Synchronization in the Visual Cortex". The Journal of Neuroscience. 24 (46): 10369–10378. doi: 10.1523/jneurosci.1839-04.2004 . PMC   6730306 . PMID   15548651.
  12. 1 2 Yu-Tai, Tsai (1998). "Significant thalamocortical coherence of sleep spindle, theta, delta, and slow oscillations in NREM sleep: Recordings from the human thalamus". Neuroscience Letters. 485 (3): 173–177. doi:10.1016/j.neulet.2010.09.004. PMID   20837102. S2CID   38878252.
  13. 1 2 Jones, Edward G. (2010). "Thalamocortical dysrhythmia and chronic pain". Pain. 150 (1): 4–5. doi:10.1016/j.pain.2010.03.022. PMID   20395046. S2CID   6857894.
  14. Llinas, Rodolfo (1999). "Thalamocortical dysrhythmia: a neurological and neuropsychaitric syndrome characterized by magnetoencephalography". PNAS. 96 (26): 15222–15227. Bibcode:1999PNAS...9615222L. doi: 10.1073/pnas.96.26.15222 . PMC   24801 . PMID   10611366.