  A fundamental problem in neuroscience is understanding how a network's
properties dictate its function. Connectomics provides one avenue to predict
nervous system function. To test this explicitly, we systematically measure
signal propagation in 23,427 pairs of neurons across the head of the nematode
Caenorhabditis elegans by direct optogenetic activation and simultaneous
whole-brain calcium imaging. We measure the sign (excitatory or inhibitory),
strength, temporal properties, and causal direction of signal propagation
between these neurons to create a functional atlas. We find that signal
propagation differs from predictions based on anatomy. Using mutants, we show
that extrasynaptic signaling not visible from anatomy contributes to this
difference. We identify many instances of dense-core-vesicle dependent
signaling on seconds-or-less timescales that evoke acute calcium transients
often where no direct wired connection exists but where relevant neuropeptides
and receptors are expressed. We propose that here extrasynaptically released
neuropeptides serve a similar function as that of classical neurotransmitters.
Finally, our measured signal propagation atlas better predicts neural dynamics
of spontaneous activity than does anatomy. We conclude that both synaptic and
extrasynaptic signaling drive neural dynamics on short timescales and that
measurement of evoked signal propagation are critical for interpreting neural
function.
