HOW INDEPENDENT ARE THE MESSAGES CARRIED BY ADJACENT INFERIOR TEMPORAL CORTICAL-NEURONS

There are at least three possibilities for encoding information in a s mall area of cortex. First, neurons could have identical characteristi cs, thus conveying redundant information; second, neurons could give d ifferent responses to the same stimuli, thus conveying independent inf ormation; or third, neurons could cooperate with each other to encode more information jointly than they do separately, that is, synergistic ally. We recorded from 28 pairs of neurons in inferior temporal cortex of behaving rhesus monkeys. Each pair was recorded from a single micr oelectrode. Both the magnitude and the temporal modulation of the resp onses were quantified. We separated the responses into signal (average response to each stimulus) and noise (deviation of each response from the average). Linear regression showed that an average of only 18.7% of the magnitude of the signal carried by one neuron could be predicte d from the magnitude of the other, and only 22.0% could be predicted b y including the temporal modulation. For the noise, the figures were 5 .5% and 6.3%, respectively, even less than for the signal. Information theoretic analysis shows that the pairs of neurons we studied carried an average of 20% redundant information. However, even this relativel y small amount of redundancy places a severe upper limit on the inform ation that can be transmitted by a neuronal pool. A pool of neurons fo r which each pair is mutually redundant to extent y can only carry a m aximum of 1/y, here five times, as much information as one neuron alon e. Information theoretic analysis gave no evidence for the presence of information as a function of both neurons considered together, that i s, synergistic codes. Cross-correlation showed that at least 61% of th e neuronal pairs shared connections in some manner. Given these shared connections, if adjacent neurons had had identical characteristics, t hen the noise on the outputs of these neurons would have been highly c orrelated, and it would not be possible to separate the signal and noi se. The severe impact of correlated noise and information redundancy l eads us to propose that the processing carried out by these neurons ev olved both to provide a rich description of many stimulus properties a nd simultaneously to minimize the redundancy in a local group of neuro ns. These two principles appear to be a major constraint on the organi zation of inferior temporal, and possibly all, cortex.