ABSTRACT
Several mammalian-based theories propose that the varying patterns of neuronal activity occurring in wakefulness and sleep reflect different modes of information processing. Neocortical slow-waves, hippocampal sharp-wave ripples, and thalamocortical spindles occurring during mammalian non-rapid eye-movement (NREM) sleep are proposed to play a role in systems-level memory consolidation. Birds show similar NREM and REM (rapid eye-movement) sleep stages to mammals; however, it is unclear whether all neurophysiological rhythms implicated in mammalian memory consolidation are also present. Moreover, it is unknown whether the propagation of slow-waves described in the mammalian neocortex occurs in the avian "cortex" during natural NREM sleep. We used a 32-channel silicon probe connected to a transmitter to make intracerebral recordings of the visual hyperpallium and thalamus in naturally sleeping pigeons (Columba livia). As in the mammalian neocortex, slow-waves during NREM sleep propagated through the hyperpallium. Propagation primarily occurred in the thalamic input layers of the hyperpallium, regions that also showed the greatest slow-wave activity (SWA). Spindles were not detected in both the visual hyperpallium, including regions receiving thalamic input, and thalamus, using a recording method that readily detects spindles in mammals. Interestingly, during REM sleep fast gamma bursts in the hyperpallium (when present) were restricted to the thalamic input layers. In addition, unlike mice, the decrease in SWA from NREM to REM sleep was the greatest in these layers. Taken together, these variant and invariant neurophysiological aspects of avian and mammalian sleep suggest that there may be associated mechanistic and functional similarities and differences between avian and mammalian sleep.
Subject(s)
Columbidae/physiology , Sleep, REM/physiology , Sleep, Slow-Wave/physiology , Visual Cortex/physiology , Animals , Birds , Brain Mapping , Electroencephalography/methods , Hippocampus/physiology , Male , Mice , Neocortex/physiology , Neurons/physiology , Thalamus/physiology , Wakefulness/physiologyABSTRACT
Auditory systems bias responses to sounds that are unexpected on the basis of recent stimulus history, a phenomenon that has been widely studied using sequences of unmodulated tones (mismatch negativity; stimulus-specific adaptation). Such a paradigm, however, does not directly reflect problems that neural systems normally solve for adaptive behavior. We recorded multiunit responses in the caudomedial auditory forebrain of anesthetized zebra finches (Taeniopygia guttata) at 32 sites simultaneously, to contact calls that recur probabilistically at a rate that is used in communication. Neurons in secondary, but not primary, auditory areas respond preferentially to calls when they are unexpected (deviant) compared with the same calls when they are expected (standard). This response bias is predominantly due to sites more often not responding to standard events than to deviant events. When two call stimuli alternate between standard and deviant roles, most sites exhibit a response bias to deviant events of both stimuli. This suggests that biases are not based on a use-dependent decrease in response strength but involve a more complex mechanism that is sensitive to auditory deviance per se. Furthermore, between many secondary sites, responses are tightly synchronized, a phenomenon that is driven by internal neuronal interactions rather than by the timing of stimulus acoustic features. We hypothesize that this deviance-sensitive, internally synchronized network of neurons is involved in the involuntary capturing of attention by unexpected and behaviorally potentially relevant events in natural auditory scenes.