Modulation of auditory processing by cortico-cortical feed-forward and feedback projections

Abstract

The auditory center in the cerebrum, the auditory cortex, consists of multiple interconnected areas. The functional role of these interconnections is poorly understood. The auditory cortex of the mustached bat consists of at least nine areas, including the frequency modulation-frequency modulation (FF) and dorsal fringe (DF) areas. The FF and DF areas consist of neurons tuned to specific echo delays carrying target-distance information. The DF area is hierarchically at a higher level than the FF area. Here, we show that the feedback projection from the DF area to the FF area shifts the delay-tuning of FF neurons toward that of the stimulated DF neurons. In contrast, the feed-forward projection from the FF area to the DF area shifts the delay-tuning of DF neurons away from that of the stimulated FF neurons. The lateral projection within the DF area shifts the delay-tuning of DF neurons toward that of the stimulated DF neurons. In contrast, the lateral projection within the FF area shifts the delay-tuning of FF neurons away from that of the stimulated FF neurons. The delay-tuning shift evoked by the DF stimulation was 2.5 times larger than that evoked by the FF stimulation. Our data indicate that the FF-DF feed-forward and FF-FF lateral projections shape the highly selective neural representation of the tuning of the excited DF neurons, whereas the DF-FF feedback and DF-DF lateral projections enhance the representation of the selected tuning, perhaps, for focal processing of information carried by the excited FF neurons.bat ͉ cortical electric stimulation ͉ delay tuning ͉ hearing ͉ plasticity T he auditory center in the cerebrum, the auditory cortex, consists of multiple, anatomically distinct areas, as do other sensory cortices. Its functional organization beyond tonotopy, however, has hardly been explored, except for the auditory cortex of the mustached bat, Pteronotus parnellii. Tonotopically organized cortical auditory areas are commonly interconnected (1). The cortico-cortical interaction within the primary auditory cortex has been studied (2-6). However, the cortico-cortical interaction between different cortical auditory areas has not yet been studied. The interaction between different cortical areas in a sensory system has thus far been studied only in the cat visual cortex by Galuske et al. (7). They found that inactivation of the visuoparietal cortex decreases the orientation and direction sensitivities of neurons in area 18. That is, they studied the effect of the feedback projection (the projection from a higher to a lower area in a signal processing hierarchy), but not that of the feed-forward projection (the projection from a lower to a higher area).A microchiropteran bat emits orientation sounds (biosonar pulses or, simply, pulses) and listens to their echoes for echolocation. The delay of an echo from the emitted pulse carries target-distance information. In the mustached bat, the biosonar pulse consists of a long constant frequency (CF) and a short frequency-modulated (FM) component, and these com...

Tuning shifts of the auditory system by corticocortical and corticofugal projections and conditioning

“…5e). In other words, lateral, contralateral, feedforward and/or feedback modulations by the FF area are centrifugal but those of the DF area are centripetal (Xiao and Suga 2004; Tang et al 2007; Tang and Suga 2008, 2009). In addition, it has also been known that feedback modulation of the VF area to the FF area is centripetal (Fig.…”

“…Both the DF and VF areas, subsequently found, also consist of FM-FM neurons. So, the FM-FM area is now called the FF area (Tang and Suga 2008). ]…”

The Effects of Urethane on Rat Outer Hair Cells

“…Although the time courses of the urethane-induced effects were different, all of the rats examined exhibited a similar reduction in the CM magnitude. Despite the expanding research to awake animal models of monkeys [49, 50], bats [51, 52], mice [28], and rats [53], the majority of auditory studies are based on the results obtained from anesthetized animals. The frequency selectivity of auditory neurons is composed of two elements: the frequency tuning of the cochlea and the refinement of the auditory neural system.…”

Corticocortical Interactions between and within Three Cortical Auditory Areas Specialized for Time-Domain Signal Processing

“…In the mustached bat, the cortico-cortical interaction within the primary auditory cortex has been studied (Suga and Ma, 2003 for review). However, the cortico-cortical interaction between the cortical auditory areas has been only recently studied by Tang and Suga (2008).…”

“…Both the DF and VF areas, subsequently found, also consist of FM-FM neurons. So, the FM-FM area has recently been changed to the FF area (Tang and Suga, 2008)]. In these three areas, neurons are tuned to specific echo delays and form an echo-delay axis for the systematic neural representation of target distances.…”