The brain generates coherent perceptions of objects from elementary sensory inputs. To examine how higher-order representations of smells arise from the activation of discrete combinations of glomeruli, we analyzed transformations of activity patterns between the zebrafish olfactory bulb and two of its telencephalic targets, Vv and Dp. Vv is subpallial whereas Dp is the homolog of olfactory cortex. Both areas lack an obvious topographic organization but perform complementary computations. Responses to different odors and their mixtures indicate that Vv neurons pool convergent inputs, resulting in broadened tuning curves and overlapping odor representations. Neuronal circuits in Dp, in contrast, produce a mixture of excitatory and inhibitory synaptic inputs to each neuron that controls action potential firing in an odor-dependent manner. This mechanism can extract information about combinations of molecular features from ensembles of active and inactive mitral cells, suggesting that pattern processing in Dp establishes representations of odor objects.