Is the tendency to maximise energy distribution an optimal collective activity for biological purposes? A proposal for a global principle of biological organization

Abstract

Our purpose is to address the biological problem of finding foundations of the organization in the collective activity among cell networks in the nervous system, at the meso/macroscale, giving rise to cognition and consciousness. But in doing so, we encounter another problem related to the interpretation of methods to assess the neural interactions and organization of the neurodynamics, because thermodynamic notions, which have precise meaning only under specific conditions, have been widely employed in these studies. The consequence is that apparently contradictory results appear in the literature, but these contradictions diminish upon the considerations of the specific circumstances of each experiment. After clarifying some of these controversial points and surveying some experimental results, we propose that a necessary condition for cognition/consciousness to emerge is to have available enough energy, or cellular activity; and a sufficient condition is the multiplicity of configurations in which cell networks can communicate, resulting in non-uniform energy distribution, the generation and dissipation of energy gradients due to the constant activity. The diversity of sensorimotor processing of higher animals needs a flexible, fluctuating web on neuronal connections, and we review results supporting such multiplicity of configurations among brain regions associated with conscious awareness and healthy brain states. These ideas may reveal possible fundamental principles of brain organization that could be extended to other natural phenomena and how healthy activity may derive to pathological states.

Keywords: Cognition; Consciousness; Energy gradients; Entropy; Equilibrium; Neural synchrony; Thermodynamics.

Fig. 1

Schematic plots representing the synchronization pattern in the surface of the brain (the cortex) of an epileptic patient in normal conditions (on the left) and during an ictus (epileptic seizure). The synchronization analysis was done on magnetoencephalographic signals, as described in Ref. [4]. Red colours indicate more synchrony. Note the smooth and relatively simple synchrony pattern of the ictal period, as compared with the other. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2

Conceptual analogy between pattern formation in nervous systems and in fluids. If the coherent motion of liquid molecules over macroscopic times results in the Rayleigh-Bénard convection and the hexagonal pattern, the coherent activity among brain cells over macroscopic times brings about a pattern of activity that determines a specific behaviour. All these phenomena are constrained by the environmental “boundary conditions”, so to speak. The backward arrows indicate that the macroscopic pattern in turn affects the microscopic, or local, interactions, as explained by the slaving principle of synergetics [44].

Fig. 3

The global and local views in neuroscience. Macroscopic regularity and microscopic variability during an episode of theta wave activity in a rodent brain. The upper trace is the electroencephalogram (EEG) representing global collective activity of millions of neurons and the lower trace is the simultaneous recording of the activity of a pyramidal neuron. Note the less regular pattern of the neuron's spike firing as compared with the theta rhythm in the EEG. Reproduced from Ref. [45].

Fig. 4

Configurations of connections among cell networks viewed from the perspective of energy distribution. Each dot represents a neural network and the lines their connectivity that define microstates, with the macrostate represented as the circle surrounding the microstates. For either no connectivity or all-to-all connections, the number of configurations is low (only 1), at the right and left hand side of the inverted U curve, whereas at the top the maximal number of configurations is found. This maximisation is given by a certain number of allowed connections, neither too many (moving towards the right of the curve) nor too few (towards the left of the curve); in this particular case when there are 4 networks the connectivity that gives the maximum configurations is 3 (for clarity, not all configurations are shown in the macrostate at the top). Shown as well are connectivity of 0, 1, 5 and 6 (from left to right). Considering neural connections as pathways for energy distribution, the y axis can be thought of as the configurations of energy distribution. In the original publications the y axis represented the entropy associated with the number of possible configurations, and the x axis the number of brain signals that were found “connected”, and the experimental data placed conscious states near the top and unconscious ones to the left or the right of the top [72,73].

Fig. 5

Spatio-temporal patterns as expressions of the tendency to widespread energy distribution constrained by different conditions. As stated in the text, interactions among system's elements that exchange energy result in diverse emergent properties, although the general principle is common.