The interconnected architecture of the functional units of the cerebral cortex provides an ideal excitable active medium to generate chaotic spatio-temporal patterns of neural activity ruled by the reaction-diffusion equations (see section 1.8).
In intact slices of the cortex of small experimental animals, spatio-temporal patterns of activity have been obtained by recording neural activity by multi-electrode arrays or by voltage sensitive dyes. In such slices of cerebral cortex, longer intercortical connections and connections with the subcortical centres can be interrupted, leaving intact only shorter connections between the cortical columns.
Early experiments showed localised electrical stimulation of isolated areas of cat neocortex initiates neural activity that propagates in all directions confirming that there is a high interconnectivity between the columnar units1. In rat neocortical slices, spatio-temporal maps were constructed from multiple site recordings and showed spontaneous spread of neural activity across the cortex2. These spatio-temporal maps show 8 Hz neural oscillation with propagating patterns of cyclic electrical activity, described as travelling waves, with “regular” periods (with relatively stable frequency and amplitude), and “irregular” periods (with variable frequency and amplitude)3. Elegant studies in similar preparations showed that the neurons behave as oscillatory nets with typical spatio-temporal patterns of chaotic systems4.
The chaotic waves are based on local connections and generally propagate at speeds from 0.1 to 0.8 m/s, consistent with the axonal conduction speed of the thin horizontal nerve fibres within the superficial layers of the cortex. These shorter association fibres between cortical columns thus provide the substrate for propagation of concentric, travelling, and spiral neural waves generated by the reaction-diffusion equations described above5.
Also in intact neonatal rat cerebral cortex and cortical slices, carbachol, a substance that acts like acetylcholine, one of the brain neurotransmitters, elicits neural oscillations which propagated uniformly at 0.5–1.5 mm/s over the cortex and the propagation was attributed to intracortical horizontal connections6.
Cortical slices from neocortex and hippocampus in other experimental animal species show similar spatio-temporal patterns of activity including chaotic travelling, concentric and spiral waves of neural activity7. Similar spatio-temporal patterns can also be generated by direct electrical interactions (ephaptic conduction) between neurons.
Besides the cerebral cortex, concentric and spiral propagating neural waves have also been observed in the isolated chicken retina8 and in the visual thalamus of ferrets9.
Slices comprising the lateral geniculate nucleus (LGN) part of the thalamus and the associated reticular nuclei with their intact synaptic connections, were also shown to display spontaneous chaotic travelling neural waves10.
Interestingly, waves of calcium increases also have been recorded in astrocytes mediated by the release of ATP11.
Isolated slabs of guinea-pig somatosensory cortex and rat barrel cortex show propagating neural activity initiated by local electrical stimulation. Similarly, electrical stimulation in isolated slabs of rat and cat cortex triggers propagating waves12. Patches of these cortical slices have preferred propagation directions that are mediated by excitatory horizontal connections in the cortex13.
All these results suggests that isolated slices of neocortex and other parts of the central nervous system can generate propagating waves of activity, in some cases, across primary, secondary and association cortices. These preparations behave as weakly coupled oscillating units typical of symmetrical-isometrical active media and can generate chaotic spatio-temporal patterns of neural activity following the rules of reaction-diffusion equations. The most suitable way to study the patterns of neural activity is to represent them as four-dimensional structures in digital spatio-temporal maps.
- BD Burns (1951): Some properties of the cat’s isolated cerebral cortex. Journal of Physiology 111, 50-68;
BD Burns et al (1957): Identification of neurones giving burst response in isolated cerebral cortex. Journal of Neurophysiology 20, 200-210. ↩︎ - JC Wester, D Contreras, D (2012): Columnar interactions determine horizontal propagation of recurrent network activity in neocortex. Journal of Neuroscience 32, 5454– 5471. ↩︎
- W Bao, JY Wu (2003): Propagating wave and irregular dynamics: spatiotemporal patterns of cholinergic theta oscillations in neocortex in vitro. Journal of Neurophysiology 90, 333–341 ↩︎
- XY Huang et al (2004): Spiral Waves in Disinhibited Mammalian Neocortex. Journal of Neuroscience, 24, 9897-9902. ↩︎
- Keane A & Gong P (2015): Propagating waves can explain irregular neural dynamics. Journal of Neuroscience 35, 1591–1605. ↩︎
- W Kilb & HJ Luhmann (2003): Carbachol-induced network oscillations in the intact cerebral cortex of the newborn rat. Cerebral Cortex13, 409–421. ↩︎
- A Compte et al (2003): Cellular and network mechanisms of slow oscillatory activity (~1 Hz) and wave propagations in a cortical network model. Journal of Neurophysiology 89, 2707–2725;
D Golomb & Y Amitai (1997): Propagating neuronal discharges in neurocortical slices: computational and experimental study. Journal of Neurophysiology 78, 1199 –1211;
MV Sanchez-Vive, DA McCormick (2000): Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nature Neuroscience 3, 1027–1034. ↩︎ - N A Gorelova, J Bures (1983): Spiral waves of spreading depression in the isolated chicken retina. Journal of Neurobiology 14, 353-363. ↩︎
- U Kim et al (1995): Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. Journal of Neurophysiology 74, 1301–1323. ↩︎
- M von Krosigk et al (1993): Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261, 361–364. ↩︎
- PB Guthrie et al (1999): ATP released from astrocytes mediates glial calcium waves. Journal of Neuroscience 19, 520–528. ↩︎
- D Contreras,R Llinas (2001) Voltage-sensitive dye imaging of neocortical spatiotemporal dynamics to afferent activation frequency. Journal of Neuroscience 21, 9403–9413;
JY Wu et al (1999): Propagating activation during oscillations and evoked responses in neocortical slices. Journal of Neuroscience 19, 5005–5015;
RD Chervin et al (1988): Periodicity and directionality in the propagation of epileptiform discharges across neocortex. Journal of Neurophysiology 60, 1695–1713. ↩︎ - Y Chagnac-Amitai & BW Conners (1989): Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. Journal of Neurophysiology 61, 747– 758. ↩︎