Information coding in the cortex by independent or coordinated populations.

The cerebral cortex is the primary seat of our sensory experiences, our plans, and the control of our actions. As such, it has been carefully examined since the inception of brain science and has been studied intensively at the level of individual neurons for over 40 years (1, 2). Nonetheless, it appears a fair assessment to say that the single most essential question about cortical physiology—‘‘What is the basic cortical population signalling mechanism? ’’—has not yet been definitively answered and is still the subject of vigorous debate (3–9). Does the cortex function by pooling together essentially independent neural signals, as in an election, or does the signal come through the coordination of the elements, as in a symphony (3, 10, 11)? An article by Hatsopoulos et al., appearing in this issue of the Proceedings (12), provides interesting new examples of pairs of neurons in the primary motor cortex of monkeys conveying information by the relative timing of their action potentials during an eight-choice reaching task. Forming clear distinctions between independent and coordinated coding is challenging, because cortical neurons have overlapping functions and work together by distributing signals across many elements. These authors present a straightforward, measurable distinction between information transmission in independent and coordinated coding and use their data to evaluate these two hypotheses. The Independent Coding Hypothesis. Independent coding suggests that each cortical neuron represents a separate signal. Cortical neurons in both sensory and motor systems are broadly tuned for features of the world, with a given sensory stimulus or motor act engaging very large numbers of cortical neurons (4, 6, 10, 13). Whatever the relevant size of cortical populations, the essential feature captured by the independent coding hypothesis is that all of the information that can possibly be obtained from one neuron can be obtained from that one neuron alone, without reference to the activities of any others. Independent signals may be noisy, overlapping, or redundant and may need to be averaged or pooled to become clear, but they are carried independently. One well known sensory example is the activity of neurons in cortical area MT during the performance of motion discrimination tasks by monkeys. Individual neurons in this area have been shown to have selectivities for visual motion that parallel the perceptual performance of the animal. These data show that there can be sufficient information available to complete a particular discrimination task in the independent signals of single neurons (8, 14). However, this does not indicate whether there is more information available in the coordination of populations of these neurons, perhaps information necessary for more complex tasks or tasks requiring a more rapid solution. A well studied example of independent population coding in the primary motor cortex is the population vector method for computing predicted movement direction from the activities of a large number of independently recorded motor neurons (13, 15–17). Each neuron is presumed to ‘‘vote’’ independently for its own preferred direction of movement or for its full direction tuning curve in more modern implementations (18). The population vector method represents an independent population code, not a coordinated code, as defined below. As in the previous example, these methods do not tell us whether additional information is available in the coordinated activity of these populations. The Coordinated Coding Hypothesis. The coordinated coding hypothesis suggests that messages in the cortex are conveyed at least in part by the relative timing of the action potentials of a population of neurons. To understand the signal from each neuron, the cortex has to listen to other neurons at the same time. The defining characteristic of coordinated coding is that the signal must be derived from the relations between multiple neurons in a population, whether this relation is synchrony or any other pattern; it is not derived by tallying the independent votes of the individuals. There are now a number of cases in which cortical neurons have been shown to convey information by their relative timing when information is absent in their independent firing rate signals (9, 11, 19–22). For example, data have demonstrated that temporally coordinated action potentials can systematically signal sensory object features, even in the absence of changes in firing rate (19). Many auditory cortical neurons in anesthetized monkeys do not change their mean firing rates during the ongoing phase of continuous stimuli, so independent firing rate coding can be largely excluded for the neurons being studied in this special circumstance. Auditory cortical neurons can change their rate of synchronous spikes in this condition, and changes in synchrony are stimulus-frequency specific, are mapped systematically across the cortical surface, and follow the timecourse of ongoing stimuli. These data from a sensory system address very similar questions to those raised by Hatsopoulos et al. in the motor system—both explore systematic representation of features by cortical spikes synchronized on a timescale of 5–15 ms in the absence of parallel increases in firing rate. Special case examples in which firing rates are unchanged are particularly interesting because they can cleanly demonstrate coordinated signaling in the absence of independent firing rate signaling. It is presumed that the same coordinated signaling mechanisms might be used in more general circumstances, when firing rates are changed. Related examples also have been found in the frontal and motor cortex (23–26). Vaadia et al. found that neurons in the frontal cortex of monkeys performing a motor task could show changes in their number of synchronous spikes in relation to behavior, even in the absence of changes in mean firing rate (27). There also have been examples shown of frontal cortical neurons emitting patterns of synchronous spikes in relation to behavior (11, 27). Independent and coordinated signaling typically are found intermixed, and it is often not clear how to separate the two. For example, at stimulus or movement onsets, many neurons fire a burst of action potentials and thereby signal these events independently. However, the spikes are nearly coincident, so the relevant signal also could be the synchronous burst across