Animals smelling in the real world use a small number of receptors to sense a vast number of natural molecular mixtures, and proceed to learn arbitrary associations between odors and valences. Here, we propose how the architecture of olfactory circuits leverages disorder, diffuse sensing and redundancy in representation to meet these immense complementary challenges. First, the diffuse and disordered binding of receptors to many molecules compresses a vast but sparsely-structured odor space into a small receptor space, yielding an odor code that preserves similarity in a precise sense. Introducing any order/structure in the sensing degrades similarity preservation. Next, lateral interactions further reduce the correlation present in the low-dimensional receptor code. Finally, expansive disordered projections from the periphery to the central brain reconfigure the densely packed information into a high-dimensional representation, which contains multiple redundant subsets from which downstream neurons can learn flexible associations and valences. Moreover, introducing any order in the expansive projections degrades the ability to recall the learned associations in the presence of noise. We test our theory empirically using data from Drosophila. Our theory suggests that the neural processing of sparse but high-dimensional olfactory information differs from the other senses in its fundamental use of disorder.
Biological intelligence is remarkable in its ability to produce complex behavior in many diverse situations through data efficient, generalizable, and transferable skill acquisition. It is believed that learning “good” sensory representations is important for enabling this, however there is little agreement as to what a good representation should look like. In this review article we are going to argue that symmetry transformations are a fundamental principle that can guide our search for what makes a good representation. The idea that there exist transformations (symmetries) that affect some aspects of the system but not others, and their relationship to conserved quantities has become central in modern physics, resulting in a more unified theoretical framework and even ability to predict the existence of new particles. Recently, symmetries have started to gain prominence in machine learning too, resulting in more data efficient and generalizable algorithms that can mimic some of the complex behaviors produced by biological intelligence. Finally, first demonstrations of the importance of symmetry transformations for representation learning in the brain are starting to arise in neuroscience. Taken together, the overwhelming positive effect that symmetries bring to these disciplines suggest that they may be an important general framework that determines the structure of the universe, constrains the nature of natural tasks and consequently shapes both biological and artificial intelligence.
Perceptual constancy refers to the fact that the perceived geometrical and physical characteristics of objects remain constant despite transformations of the objects such as rigid motion. Perceptual constancy is essential in everything we do, like recognition of familiar objects and scenes, planning and executing visual navigation, visuomotor coordination, and many more. Perceptual constancy would not exist without the geometrical and physical permanence of objects: their shape, size, and weight. Formally, perceptual constancy and permanence of objects are invariants, also known in mathematics and physics as symmetries. Symmetries of the Laws of Physics received a central status due to mathematical theorems of Emmy Noether formulated and proved over 100 years ago. These theorems connected symmetries of the physical laws to conservation laws through the least-action principle. We show how Noether's theorem is applied to mirror-symmetrical objects and establishes mental shape representation (perceptual conservation) through the application of a simplicity (least-action) principle. This way, the formalism of Noether's theorem provides a computational explanation of the relation between the physical world and its mental representation.
First, neurophysiological evidence for the learning of invariant representations in the inferior temporal visual cortex is described. This includes object and face representations with invariance for position, size, lighting, view and morphological transforms in the temporal lobe visual cortex; global object motion in the cortex in the superior temporal sulcus; and spatial view representations in the hippocampus that are invariant with respect to eye position, head direction, and place. Second, computational mechanisms that enable the brain to learn these invariant representations are proposed. For the ventral visual system, one key adaptation is the use of information available in the statistics of the environment in slow unsupervised learning to learn transform-invariant representations of objects. This contrasts with deep supervised learning in artificial neural networks, which uses training with thousands of exemplars forced into different categories by neuronal teachers. Similar slow learning principles apply to the learning of global object motion in the dorsal visual system leading to the cortex in the superior temporal sulcus. The learning rule that has been explored in VisNet is an associative rule with a short-term memory trace. The feed-forward architecture has four stages, with convergence from stage to stage. This type of slow learning is implemented in the brain in hierarchically organized competitive neuronal networks with convergence from stage to stage, with only 4-5 stages in the hierarchy. Slow learning is also shown to help the learning of coordinate transforms using gain modulation in the dorsal visual system extending into the parietal cortex and retrosplenial cortex. Representations are learned that are in allocentric spatial view coordinates of locations in the world and that are independent of eye position, head direction, and the place where the individual is located. This enables hippocampal spatial view cells to use idiothetic, self-motion, signals for navigation when the view details are obscured for short periods.