Procedural Performance Benefits after Excitotoxic Hippocampal Lesions in the Rat Sequential Reaction Time Task

Abstract

It is widely agreed upon that hippocampal function is linked to episodic-like and spatial memory across various species, for example, rodents. However, the interplay between hippocampal function and other types of learning and memory, like procedural stimulus-response or sequential learning, is less clear. Recently (Eckart et al. in Hippocampus 22:1202-1214, 2012), we showed that excitotoxic hippocampal lesions, which mainly affected its dorsal part, led not only to the expected deficits in a spatial and episodic-like memory task, namely the object place recognition test, but also to substantial improvements in terms of speed and accuracy in a rat adaption of the human sequential reaction time task (SRTT). The design of that experiment, however, which included fixed test durations per training day, led to the fact that lesioned animals gained more instrumental experience, which may partly have accounted for their enhanced performance. In order to rule out such a potential confound, we performed the present experiment on rats with similar ibotenic lesions aiming at the dorsal hippocampus, but we now kept the amount of correct instrumental responses and reinforcements on the same level as in controls. Our data revealed that lesioned animals were still able to complete the SRTT in a substantially smaller amount of time, when compared to control and sham-operated animals, although no differences were observable in terms of speed or accuracy. Also, the animals with lesions showed impaired extinction in a subsequent test where rewards were omitted. The former effect can primarily be attributed to shorter post-reinforcement pauses in the lesioned animals, and the possible mechanisms of this and the extinction effect will be addressed in the discussion.

Decoupling Actions from Consequences: Dorsal Hippocampal Lesions Facilitate Instrumental Performance, but Impair Behavioral Flexibility in Rats

“…Surgery was performed similarly to our previous study: animals were anesthetized with isoflurane (Baxter Deutschland GmbH, Germany) and coordinates from bregma, as well as injection volumes for dHC lesion were identical to our previous study (for details, see Busse and Schwarting, 2016 ). Ibotenic acid and saline injections were made using a home-made injection system with a 1 μl SGE syringe (SGE Analytical Science), that was connected via polyethylene tubing (0.38 mm × 1.09 mm diameter; Plastics One Inc., VA, USA) to the injection cannula (gauge 26, Plastics One Inc., VA, USA).…”

“…Ibotenic acid and saline injections were made using a home-made injection system with a 1 μl SGE syringe (SGE Analytical Science), that was connected via polyethylene tubing (0.38 mm × 1.09 mm diameter; Plastics One Inc., VA, USA) to the injection cannula (gauge 26, Plastics One Inc., VA, USA). In order to allow the ibotenic acid or saline to diffuse, the syringe was kept in place for about 1–2 min after each injection (Busse and Schwarting, 2016 ).…”

“…Similar to what is known from patients with Parkinson’s disease (Ferraro et al, 1993 ; Nagy et al, 2007 ; Carbon et al, 2010 ), our early studies had shown that striatal dopamine lesions led to behavioral deficits (Domenger and Schwarting, 2008 ; Eckart et al, 2010 ). In contrast, and rather surprisingly, lesions of the dorsal hippocampus (dHC) led to substantial improvements, that is, they actually boosted performance in the SRTT (Eckart et al, 2012 ; Will et al, 2013 ; Busse and Schwarting, 2016 ). Thus, in our first dHC lesion study, where we analyzed sequential learning and performance, we found that rats with excitotoxic dHC lesions showed clearly faster reaction times (RTs) and higher response accuracy (ACC) as compared to controls.…”

“…This factor may have favored learning and performance in rats with dHC lesions, which, due to their faster performance, obtained more practice each day. In order to rule this factor out, we performed another study (Busse and Schwarting, 2016 ), where daily training was ended whenever the rats had achieved a fixed number of successful instrumental responses and thus rewards. Again, rats with dHC lesions had deficits in an object-place recognition task, showing their typical declarative deficits.…”

“…In this task, sequences of distinct visual stimulus presentations are food-rewarded in a fixed-ratio-13-schedule. Our previous study (Busse and Schwarting, 2016 ) had shown that rats with lesions of the dHC show substantially shorter session times and post-reinforcement pauses (PRPs) than controls, which allows for more practice when daily training is kept constant. Since sequential behavior is based on instrumental performance, a sequential benefit might be secondary to that.…”