Gareth Leng

“We must consider what we mean when we say that the spiking activity of a neuron 'encodes' information. We normally think of a code as something that conveys information from a sender to a recipient, and this requires that the recipient 'understands' the code. But the spiking activity of every neuron seems to encode information in a slightly different way, a way that depends on that neuron's intrinsic properties. So what sense can a recipient make of the combined input from many neurons that all use different codes? It seems that what matters must be the 'population code' - not the code that is used by single cells, but the average or aggregate signal from a population of neurons.
In a now classic paper, Shadlen and Newsome considered how information is communicated among neurons of the cortex - neurons that typically receive between 3,000 and 10,000 synaptic inputs.They argued that, although some neural structures in the brain may convey information in the timing of successive spikes, when many inputs converge on a neuron the information present in the precise timing of spikes is irretrievably lost, and only the information present in the average input rate can be used. They concluded that 'the search for information in temporal patterns, synchrony and specially labeled spikes is unlikely to succeed' and that 'the fundamental signaling units of cortext may be pools on the order of 100 neurons in size.' The phasic firing of vasopressin cells is an extreme demonstration of the implausibility of spike patterning as a way of encoding usable information, but the key message - that the only behaviorally relevant information is that which is collectively encoded by the aggregate activity of a population - may be generally true.”
― Gareth Leng, The Heart of the Brain: The Hypothalamus and Its Hormones

“What we have seen does not sit comfortably with conventional views of the brain. Electrophysiology has been a powerful tool and its returns have permeated our thinking about how the brain works, but the resulting understanding is cursed by overinterpretation. Because spike activity appears to have so much capacity for encoding information, we are tempted to think it in fact conveys a huge volume of information. When we find, in the spike activity of some neuron or another, correlation between some facet and some particular external events, it is tempting to think this is the message the cell is conveying.
A message is only a message if it can be understood by its recipient. Neurons can't decipher long and complex sentences. They have a short attention span, are easily distracted, and much of the time they aren't even listening. A neuron that is quiet at a particular time is likely also to be less sensitive to an input; a cell that is very active might be saturated; and a cell recently activated might be refractory to further activation.
Spike activity is not the output of any neuron, only one of several means by which some of its chemical signals are generated. These signals are generated unreliably and erratically and are recognized imperfectly by their targets. The message carried by the spike activity of a vasopressin cell makes no sense when considered alone. The important signal is generated by a cacophony of noisy and messy cells , and the miracle that demands to be recognized is that this population response is indeed clean, refined and fit for purpose.”
― Gareth Leng, The Heart of the Brain: The Hypothalamus and Its Hormones