I will admit I have never thought about the question: how many spikes is your brain emitting every second? And how many could it emit? Lucy notwithstanding, it is probably something less than ‘all of them’. Beyond the obvious “that is called epilepsy”, there is also an unappreciated metabolic constraint. Spiking is costly! How much could the brain spike?
Let’s think about how we can estimate this. First you have to know how much energy a single spike would ‘cost’ the brain. Every spike is the result of an ebb and flow of sodium and potassium (et al) ions through the pores in the cell. The net result is an unbalancing of these ions which need to be actively pumped out. Additionally, every spike is caused by EPSPs which also require the neuron to expend energy. A spike traveling down the axons is costly. Exocytosis and endocytosis of neurotransmitters requires energy. Sum these all up and you can get some energy requirement: precisely how much energy you need in order to sustain a single spike. In terms of ATP, the unit of energy in biology, we get something on the order of 2.4 * 10^9 molecules of ATP needed for each one!
Once we estimate this, we can ask how much energy the brain consumes as a whole. PET scans are able to estimate the amount of glucose the brain is consuming, and this turns out to be about 77 mg/min, or 34 mg/min for the neocortex (meaning neocortex alone uses 44% of the brain’s energy!). Converting to ATP, we get about 3.4 * 10^21 molecules of ATP per minute. Finally, we do a bit of division and we can guess that cortex is emitting 3,360,000,000 spikes per second – so each neuron is spiking only once every six seconds!
How high could we push this spike rate? If the cortex was spiking at a measly 1.8 Hz, it would use more energy than the whole brain. If it were spiking at 13 Hz, it would use more energy than the whole body!
Just from metabolic constraints we can ask how sparse the activity in the brain is. Simply put, as the average spike rate in ‘active’ neurons goes up, the number of neurons that the brain can support goes down. If neurons were to fire a single spike in a single second, then only 0.1-1% of neurons could be active at all.
Not every neuron is the same, though. Neurons aren’t just chattering away at each other but are actually trying to communicate something, each in their own special way. Some are especially chatty in their attempts to shut down the signaling of other cells and spike really quickly. These are given the imaginative name of “fast spiking interneurons”. One fancy feature of these fast spikers is that they have very narrow action potentials in order to maximize how fast they can go.
But this ability comes with a cost: energy. In order to end each spike quickly, the cell has very quick and powerful potassium channels that drive the membrane potential down. Look at the figure just below. In the second row, you can see a model of the sodium and potassium currents. There is so much more going on when the spike is narrower (right) than when it is broad (left). This means that these cells not only fire more, but each time they do that they consume more energy.
If these neurons are firing so much, and using so much energy, how little must the other neurons be spiking? Does the average spike rate for non-fast spikers go down from 0.16Hz to 0.016Hz? Does the number of active excitatory cells go from maybe 0.5% all the way to 0.05%?
Lennie, P. (2003). The Cost of Cortical Computation Current Biology, 13 (6), 493-497 DOI: 10.1016/S0960-9822(03)00135-0
Hasenstaub, A., Otte, S., Callaway, E., & Sejnowski, T. (2010). Metabolic cost as a unifying principle governing neuronal biophysics Proceedings of the National Academy of Sciences, 107 (27), 12329-12334 DOI: 10.1073/pnas.0914886107