Parallel pathways in retina send information efficiently

Visual information is sent from eye to brain by ∼15 types of ganglion cell. Because the retina is constrained for energy, we hypothesized that this \u27parallel pathways\u27 design is energy-efficient. To test this, we estimated for several types of ganglion cell: (i) information efficiency (ratio of information rate to coding capacity); (ii) \u27natural information rate\u27 (bit rate to natural movies); (iii) metabolic cost per unit information. We recorded spikes (in vitro guinea pig) while presenting white noise or natural movies. By calculating, for the observed spike rate, the number of possible spike patterns, we calculated coding capacity, and by counting the number of actual spike patterns, we estimated information rate. For every cell type, information rate was ∼one-third of coding capacity; all types were equally efficient. Due to higher coding capacity, the \u27natural information rate\u27 of brisk cells was twice that of sluggish (13 vs. 6 bits s-1). To estimate bit cost, we first calculated information per spike. Sluggish spikes conveyed ∼20% more information than brisk spikes (2.2 vs. 1.8 bits). Next, we estimated spike cost by measuring charge carried by an excitatory quantum, the number of quanta that trigger a spike, and charge moved during the spike voltage change. We converted charge to ATP used by the Na +/K+ATPase. The dominant cost was the spike voltage change (quanta contributed only ∼10%). A brisk-transient spike moved the most charge and therefore must use the most ATP. Spike cost divided by information per spike gave bit cost. Bit cost and bit rate were linearly related; a brisk-transient bit costs twice that of sluggish (∼5×107 vs. 3×107 ATP molecules). Finally, knowing densities of each cell type, we estimated the amount of information sent from eye to brain and the corresponding metabolic cost (at ganglion cell level). The guinea pig eye sends ∼875,000 bits s-1 at a cost of ∼3×10 13 ATP molecules. Sluggish cells, being the most numerous, account for the majority of information (64%). To send information exclusively via high-rate brisk-transient cells would cost nearly twice as much. Parallel pathways increase efficiency by enabling the trade-off between bit rate and bit cost